| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
The Journal of Neurophysiology Vol. 80 No. 4 October 1998, pp. 2015-2022
Copyright ©1998 by the American Physiological Society
1 Respiratory Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta T2N 4N1, Canada; and 2 Division of Life Sciences, University of Texas at San Antonio, San Antonio, Texas 78249
 |
ABSTRACT |
|---|
 Abstract
 Introduction
Methods
Results
Discussion
References
|
|---|
Torgerson, C. S., M. J. Gdovin, and J. E. Remmers. Fictive gill and lung ventilation in the pre- and postmetamorphic tadpole brain stem. J. Neurophysiol. 80: 2015-2022, 1998. The pattern of efferent neural activity recorded from the isolated brain stem preparation of the tadpole Rana catesbeiana was examined to characterize fictive gill and lung ventilations during ontogeny. In vitro recordings from cranial nerve (CN) roots V, VII, and X and spinal nerve (SN) root II of premetamorphic tadpoles showed a coordinated sequence of rhythmic bursts occurring in one of two patterns, pattern1, high-frequency, low-amplitude bursts lacking corresponding activity in SN II and pattern 2, low-frequency, high-amplitude bursts with coincident bursts in SN II. These two patterns corresponded to gill and lung ventilatory burst patterns, respectively, recorded from nerve roots of decerebrate, spontaneously breathing tadpoles. Similar patterns were observed in brain stem preparations from postmetamorphic tadpoles except that they showed a greater frequency of lung bursts and they expressed fictive gill ventilation in SN II. The laryngeal branch of the vagus (Xl) displayed efferent bursts in phase with gill and lung activity, suggesting fictive glottal constriction during gill ventilation and glottal dilation during lung ventilation. The fictive gill ventilatory cycle of pre- and postmetamorphic tadpoles was characterized by a rostral to caudal sequence of CN bursts. The fictive lung ventilatory pattern in the premetamorphic animal was initiated by augmenting CN VII discharge followed by synchronous bursts in CN V, X, SN II, and Xl. By contrast, postmetamorphic patterns of fictive lung ventilation were characterized by lung burst activity in SN II that preceded burst onset in CN V and followed the lead burst in CN VII. We conclude that recruitment and timing of pattern 1 and pattern 2 rhythmic bursts recorded in vitro closely resemble that recorded during spontaneous respiratory behavior, indicating that the two patterns are the neural equivalent of gill and lung ventilation, respectively. Further, fictive gill and lung ventilatory patterns in postmetamorphic tadpoles differ in burst onset latency from premetamorphic tadpole patterns and resemble fictive oropharyngeal and pulmonary burst cycles in adult frogs.
The assumption of terrestriality by vertebrates required profound changes in the form and function of the respiratory system associated with the transition from water to air (see reviews by Dejours 1988
General
Experiments were performed on 17 larval bullfrog tadpoles (R. catesbeiana) of either sex, obtained from a commercial supplier (Charles D. Sullivan, Nashville, TN). Specimens were assigned to one of two groups based on the criteria of Taylor and Köllros (1946), premetamorphic (stages 4-14, n = 10,) and postmetamorphic (stages 20-22, n = 7). During the 5 days preceding experimentation, all tadpoles were housed in aerated, filtered aquariums (19-21°C) and fed TetraFin Staple Food (TetraWerke, Germany). The Animal Care Committee of the University of Calgary, Canada, approved the experimental protocol used in these studies.
Surgical preparation
Tadpoles were anesthetized in tricaine methane sulfonate (1:10,000) and then weighed. Once unresponsive, the dorsal cranium was removed, and with the aid of a dissecting microscope the cranial and SNs were severed at their respective ostia. After removing the dura and arachnoid dorsally and ventrally, the brain stem was transected just caudal to the level of the fourth SN and just rostral to CN V. In a subset of premetamorphic tadpoles (n = 3), Xl, which innervates glottal constrictors and dilators, was dissected and left attached to the brain stem. In these animals, the main trunk of the vagus was freed dorsally by resection of the cartilage surrounding the postotic foramen and by careful excision of the dorsolateral margin of the semicircular canal. Using a ventral approach, Xl was exposed by excising the overlying tissue and isolating the entire nerve. Throughout the dissection, the brain stem was superfused with a bicarbonate containing artificial cerebrospinal fluid (CSF) of the following composition (in mM): 104 NaCl, 4 KCl, 1.4 MgCl2, 10 D-glucose, 25 NaHCO3, and 24 CaCl2, bubbled with 98% O2-2% CO2, pH 7.8, corresponding to the plasma pH of anuran amphibians (West et al. 1987 Recording chamber
The brain stem was transferred to a superfusion recording chamber that was described previously (Torgerson et al. 1997b Recording
Efferent recordings were obtained from the roots of CN V, VII and X, SN II (hypoglossal in the adult), and Xl by using suction electrodes. The pipettes were made from 1-mm OD, thin-walled borosilicate glass and then pulled to a fine tip with a horizontal micropipette puller (Brown-Flaming, model P80). The tip was broken and beveled (Shöhli, Lapp-Technik) to achieve various inner tip diameters ranging from 90 to 350 µm. Action potentials were amplified (AM Systems no.1700, Tektronix AM 502), filtered (100 Hz to 1 kHz), and recorded on videotape with a pulse code modulator (Neurodata DR-890). The signals were simultaneously averaged with a Paynter time averager, displayed on a polygraph (Gould), and digitized and analyzed on a Pentium PC (Datapac II software).
Analysis
As described in RESULTS, gill and lung bursts were identified by SN II amplitude criteria and by correlations with the SN II recordings described by Gdovin et al. (1998) Rhythmic, coordinated bursting patterns were recorded from CN V, VII, X, SN II, and Xl in premetamorphic (n = 10) and postmetamorphic (n = 6) larvae when superfused with artificial CSF of pH 7.8 and 7.4. Although simultaneous recordings of all nerves were not successful in all animals, rhythmic bursts were recorded in two or more of the nerves in each experiment. Table 1 provides the number of animals in which each nerve as successfully recorded.
Bursting patterns
As illustrated in Fig. 1, integrated neurograms of CN V, VII, and X from a premetamorphic tadpole revealed two different patterns of rhythmic activity, high burst frequency, low-amplitude bursts (pattern 1) and low burst frequency, high-amplitude bursts (pattern 2). Figure 2 shows both unprocessed and integrated neurograms of CN V, VII, and X in a premetamorphic (stage 4) tadpole, demonstrating patterns 1 and 2. Examination of action potentials in all three nerve records indicates the recruitment of new motor units during pattern 2, as described by Gdovin et al. (1998)
Latency and time-to-peak of bursts
PREMETAMORPHIC ANIMALS.
Mean time to peak and latency values of patterns 1 and 2 are displayed in Fig. 6 and listed in Table 1. The pattern 1 ventilatory cycle of premetamorphic tadpoles was characterized by sequential bursts in CN V, VII, and X roots, with activity in Xl occurring in phase with CN VII (Fig. 6A, solid bars). Onset latency of CN V, VII, and X differed significantly (P < 0.05) from each other as well as the onset of Xl in comparison with CN V and CN X. By contrast, pattern 2 cycles in premetamorphic tadpoles began with slowly augmenting CN VII discharge that burst synchronously with CN V, X, SN II, and Xl (Fig. 6A, open bars). The onset of the pattern 2 bursts in CN V, X, Xl, and SN II significantly lagged behind (P < 0.05) the onset of lung activity in CN VII. Premetamorphic tadpoles showed no significant difference (P > 0.05) in the time to peak of cranial and SN bursts when comparisons were made within pattern 1 and 2 ventilatory cycles.
POSTMETAMORPHIC ANIMALS.
Pattern 1 in postmetamorphic larvae was distinguished by the emergence of SN II discharge that burst after sequential activation of CN V, VII, and X (Fig. 6B, filled bars). The relative mean onset latency of CN V, VII, X, and SN II bursts all differed significantly (P < 0.05) with respect to each other. The time to peak of CN VII bursts was significantly greater (P < 0.05) than the time to peak in CN V, X, and SN II bursts, and the time to peak of SN II burst activity was significantly greater (P < 0.05) than that of CN V and X. Further, the time to peak of CN VII pattern 1 bursts of postmetamorphic larvae was significantly greater (P < 0.05) than that of premetamorphic tadpoles.
Recordings of efferent activity from the roots of CN V, VII, X, SN II, and from the respiratory nerve Xl in the isolated brain stem preparation of larval R. catesbeiana displayed two types of rhythmic bursting: pattern 1, a high-frequency, low-amplitude oscillation in a rostral-to-caudal sequence, and pattern 2, a low-frequency, high-amplitude rhythm initiated by CN VII and lacking the rostral-to-caudal progression (Figs. 1-5). Pattern 1 was virtually identical in pre- and postmetamorphic animals with the exception that the latter included an oscillation in SN II. Pattern 2 was similar in pre- and postmetamorphic larvae but exhibited distinct differences in the burst latency between nerves. These patterns bear a striking resemblance to those recorded by Gdovin et al. (1998)
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Gans 1970; Little 1983; Randall et al. 1981; Shelton et al. 1986). Amphibians, modern descendents of the early tetrapods that migrated from water to land, developed complex respiratory processes and structures in response to differences in the physical properties of air and water. This is particularly apparent in larval forms where gas exchange occurs at multiple sites (skin, gills, and lungs), allowing simultaneous exploitation of both respiratory media. Investigation of the ontogeny of respiratory rhythm generation in the tadpole provides a unique opportunity to examine the development of basic neuronal processes that generate and regulate respiratory motor output.
). As body mass and metabolic demand increase, tadpoles require progressively more efficient gas exchange organs (gills and lungs). The gills are ventilated by a constant, unidirectional stream of water drawn into the mouth, through the oropharyngeal cavity, and out of the opercular spout by rhythmic dorsoventral movement of the buccal floor (DeJongh 1968). By contrast, tidal flow of air into and out of the paired, saclike lungs is accomplished by the same buccal musculature, drawing air in the oropharynx and forcing it into the lungs (Burggren 1984). Lung inflation occurs during the brief opening of the glottis and remains full until the beginning of the next cycle when exhalation, powered by elastic recoil of the respiratory system, drives the air out of the lungs. Before onset of metamorphosis (Taylor-Köllros stage 16), ventilatory patterns appear homologous to those described for lungfish, regular branchial movements pumping water over the gills and interspersed with irregular lung breaths (McMahon 1969; Smatresk 1990). During metamorphic climax (stage 18-19), the gills and tail degenerate and the lungs become the dominant site for O2 exchange, reaching full maturity in stages 20-25 (Burggren and West 1982). On completion of metamorphosis, the forelimbs develop, the gills and tail are completely reabsorbed, and the branchial cavity is filled with air between breaths (Smatresk 1990).
,b) was elucidated by correlating CN root activity with activity of nerves to respiratory muscles in an in situ preparation (Kimura et al. 1997) and with neurograms, electromyograms, and mechanical events related to oropharyngeal and pulmonary ventilatory cycles from in vivo preparations (DeJongh and Gans 1969; Ito and Watanabe 1962; Kogo et al. 1994a; Kogo and Remmers 1994b; Sakakibara 1984a,b; West and Jones 1975). Similarly, recent studies of in vitro tadpole brain stem preparations began to characterize the patterns of respiratory activity related to gill and lung ventilation (Galante et al. 1996; Liao et al. 1996; Pack et al. 1993; Torgerson et al. 1997a). However, the separate identification of lung and gill ventilatory activities in these studies must be considered tentative, as an arbitrary CN amplitude criterion alone was used to identify putative gill and lung bursts in CN roots, i.e., large amplitude bursts were assumed to be fictive lung breaths, and small amplitude bursts were assumed to be fictive gill bursts. If the isolated tadpole brain stem preparation is to be utilized as a tool to investigate fundamental questions of rhythmogenesis and central chemoreception, fictive gill and lung ventilatory activity must be separately identified.
View this table:
TABLE 1.
Mean latency and time to peak of pattern 1 and 2 bursts from CN V, VII, X, SN II, and X
View larger version (21K):
[in a new window]
FIG. 1.
Moving time average of cranial nerve (CN) V, VII, and X showing patterns 1 and 2 from the isolated brainstem preparation of a stage 11 Rana catesbeiana tadpole superfusate with artificial cerebrospinal fluid (CSF) having a PCO2 of 45 Torr and pH of 7.4. The height of the respiratory bursts was measured by using arbitrary units.
), we describe the motor output of the spontaneously breathing larval Rana catesbeiana. In this study, we provide data from the isolated tadpole brain stem preparation that can be correlated with observations from the in vivo study. A second purpose is to describe ontogenetic changes in gill and lung ventilatory motor output. To achieve these two goals, we recorded efferent activity from CN roots, the second spinal nerve (SN) root and the laryngeal branch of the vagus (Xl) in pre- and postmetamorphic tadpoles. SN II innervates the hypoglossal muscles and was shown to be a marker of lung breaths in the metamorphic tadpole in vivo (Gdovin et al. 1998). Xl can be considered a respiratory nerve because its efferent activity controls the precise opening and closing of the glottal valve during lung ventilation.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
).
). Briefly, two superimposed disks (2.5-cm OD, 1-mm thickness) with central elliptical holes (2.0 × 0.5 cm) partitioned the chamber into upper and lower compartments. Fine netting (1.0-mm2 mesh) spanning the holes was attached to the upper surface of the upper and lower disks, thereby creating a space between the netting for the brain stem. The brain stem was positioned between the two nets, ventral side up, and superfused with artificial CSF (22-24°C) equilibrated with a mixture of CO2-O2. The superfusate was conducted from the opposite end of the upper compartment via a paper wick.
60 min (pH 7.8), stable nerve activities were recorded for 10 min at pH 7.8 and 7.4. Between each 10-min recording, a 5-min equilibration period ensued to allow equalization of tonometer and recording chamber pH and stabilization of the brain stem response to the new superfusate pH.
View larger version (28K):
[in a new window]
FIG. 2.
Unprocessed and integrated neurograms of CN V, VII, and X recorded from a premetamorphic (stage 4) tadpole brain stem preparation superfused with artificial CSF having a PCO2 of 45 Torr and pH of 7.4. In raw neurograms, the recruitment of new motor units during pattern 2 is clearly distinguishable. The height of the respiratory bursts was measured by using arbitrary units.
. We define the burst frequency to be the number of bursts per unit time. To evaluate developmental differences in respiratory bursting patterns from CN V, VII, X, SN II, and Xl, we measured the time to peak and relative time of onset of fictive gill and lung ventilatory bursts for each 10-min recording at pH 7.4. Mean time to peak was calculated from the onset of the burst to the time of peak amplitude, and mean latency of fictive gill and lung ventilation was determined for each nerve with respect to the onset of the CN VII burst. Mean values of gill and lung motor output for each animal were then used to calculate group means ± SE. Significant differences in the latency and time to peak of fictive gill and lung ventilation within and between each developmental group were examined with a one-way analysis of variance (ANOVA) for repeated measures, with the criterion of statistical significance at P < 0.05. A Student-Newman-Keuls test of pairwise multiple comparisons was used to test significant differences among nerves within treatment groups when ANOVA revealed significant treatment effects.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
, further substantiating the distinction between the two motor output patterns.
, we used SN II as the marker of pattern 2, whenever possible, in our analysis. Similarly, the Xl neurogram demonstrated pronounced bursting during pattern 2 but only modest activity during pattern 1, as shown in Fig. 4. This distinctive behavior of SN II and Xl neurograms during pattern 2 was consistently observed in all recordings. In 3 of 10 premetamorphic animals and 1 of 6 postmetamorphic larvae, adequate recordings were not available from SN II. Accordingly, an amplitude criterion was used to identify pattern 2 bursts in the analysis shown in Table 1.
View larger version (22K):
[in a new window]
FIG. 3.
Integrated neurograms of CN VII and spinal nerve (SN) II showing patterns 1 and 2 recorded from a postmetamorphic (stage 21) tadpole brain stem preparation superfused with artificial CSF having a PCO2 of 45 Torr and pH of 7.4. The height of the respiratory bursts was measured by using arbitrary units.
View larger version (18K):
[in a new window]
FIG. 4.
Integrated neurograms of CN VII, Xl, and SN II showing patterns 1 and 2 recorded from a premetamorphic (stage 13) tadpole brain stem preparation superfused with artificial CSF having a PCO2 of 45 Torr and pH of 7.4. The height of the respiratory bursts was measured by using arbitrary units.
View larger version (28K):
[in a new window]
FIG. 5.
Integrated neurograms of CN VII, X, and SN II recorded from premetamorphic (stage 12, A) and postmetamorphic (stage 22, B) tadpole brain stem preparations superfused with artificial CSF having a PCO2 of 45 Torr and pH of 7.4, showing transition in the pattern of fictive ventilation with development. The height of the respiratory bursts was measured by using arbitrary units.
View larger version (15K):
[in a new window]
FIG. 6.
Onset latency and time to peak profiles of pattern 1 and 2 bursts in pre- (A) and postmetamorphic (B) tadpole larvae. Mean time to peak represented by the relative length of the bars with SEs plotted on the right. Mean onset burst latency determined with respect to CN VII (outlined by gray) and indicated by the relative horizontal position of bars with standard errors shown on the left. * Significantly different from CN VII mean values within both developmental group and type of ventilation (P < 0.05); 
significantly different from CN V mean values within both developmental group and type of ventilation (P < 0.05).
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
from CN V, VII, and SN II in the spontaneously breathing decerebrate tadpole, where gill and lung ventilation were mechanically defined. Because of their close correspondence to the in vivo patterns, we classify pattern 1 as fictive gill ventilation and pattern 2 as fictive lung ventilation.
; Liao et al. 1996; Pack et al. 1993; Torgerson et al. 1997a). The use of such a criterion was not validated, and its sensitivity and specificity are suspect. This study elaborates on the work of Pack et al. (1993) by describing the use of high-amplitude SN II bursts as a sensitive marker of fictive lung ventilation. This study also describes correlates of fictive gill and lung ventilation such as the spatiotemporal characteristics as well as recruitment of Xl bursts during fictive lung ventilation. In our experience, CN burst amplitude is not adequate to identify fictive gill and lung bursts in many cases, but, when used in combination with SN II, any particular burst can be unequivocally identified as pattern 1 or pattern 2.
in pre- and postmetamorphic tadpoles. Similarly, the frequency and rostral-to-caudal sequence of pattern 1 observed here closely resembles those reported by Gdovin et al. (1998) for gill ventilation. Comparison of Fig. 6 from Gdovin et al. (1998) and Fig. 6 from this paper show both fictive gill cycles initiated by bursts in CN V followed by activity in CN VII. Further, the frequency of gill bursts in decerebrate metamorphic tadpoles during normoxia (49.3 ± 6.1 min
1) (Gdovin et al. 1998) correlates with gill burst frequency (43.0 ± 2.7 min1) previously measured in the isolated metamorphic tadpole brain stem preparation when superfused with artificial CSF of pH 7.8 (Torgerson et al. 1997a). This evidence supplements the recruitment and amplitude data discussed above and leads to the conclusion that low-amplitude, high-frequency bursts in vitro represent fictive gill ventilation.
characterized fictive lung ventilation by synchronous burst activity in CN VII and V and by the recruitment of SN II. Similarly, we observed simultaneous bursting in CN V and VII and the appearance of SN II bursts during pattern 2 in vitro, suggesting that high-amplitude, low-frequency bursts represent fictive lung activity. Fictive lung ventilation frequency, previously described in the isolated metamorphic brain stem preparation (0.2 ± 0.1 min1, artificial CSF, pH 7.8) (Torgerson et al. 1997a), matched measurements reported by Gdovin et al. (1998) in the decerebrate metamorphic tadpole under normoxic conditions (0.3 ± 0.1 min1). Although the time to peak of gill and lung bursts recorded in vitro ranged between 10 and 100% of in vivo burst time to peak measurements, correlation between both preparations was close, in view of in vitro peripheral deafferentation and gas/pH tissue status (Torgerson et al. 1997b).
; Infantino 1992) and confirms previous results from isolated premetamorphic tadpole brain stem preparations (Torgerson et al. 1997a).
,b) attributed the activation of mouth opener and pharyngeal constrictor muscles to SN motor output, the contribution of these muscles to gill ventilation was minimal based on electromyographic and pressure recordings. Further, our results agree with Taylor (1985), who reported a similar rostral-to-caudal bursting sequence in CN output during gill ventilation in studies of dogfish. Finally, we observed rhythmic activity in Xl during fictive gill ventilation that burst in phase with CN VII. Xl innervates dilator and constrictor muscles of the glottis (Sakakibara 1984a) and was previously shown to display bursting activity during fictive oropharyngeal ventilation in in vivo (Kogo et al. 1994a,b) and in situ (Kimura et al. 1997) adult bullfrog preparations. Xl activity in premetamorphic larvae during fictive gill ventilation may represent fictive glottal closure, ensuring that no water enters the lungs before being forced over the gills.
in the adult frog. Further, exclusive lung burst activity in SN II provides a specific and sensitive marker of fictive lung activity in premetamorphic tadpole, allowing clear differentiation from gill motor output.
) and adult frogs (DeJongh and Gans 1969; MacIntyre and Toews 1976; West and Jones 1975). In the adult frog, McLean et al. (1995a,b), Kogo et al. (1994a,b), and Kimura et al. (1997) recorded efferent activity from specific branches of CN V, X, and SN II innervating buccal and laryngeal muscles and characterized the fictive lung ventilatory cycle by augmenting activity in the sternohyoid branch of SN II followed by synchronous bursting in CN V, X, and the main branch of SN II. This sequential pattern resembles that observed in the postmetamorphic tadpole but contrasts with fictive lung bursts of premetamorphic animals, showing simultaneous activation of CN V, X, Xl, and SN II.
established that fictive lung bursts were unaffected by chloride-free superfusate, indicating that postsynaptic inhibition is not essential for fictive lung rhythmogenesis. Hence fictive lung breathing in the premetamorphic tadpole may be generated from a primitive lung central pattern generator (CPG) not requiring postsynaptic inhibition, whereas fictive lung bursts in the adult frog arises from a CPG containing well-developed network properties that include postsynaptic inhibition. Interestingly, Kimura et al. (1997) showed, in the in vitro adult frog brain stem, the dependency of fictive lung ventilation on postsynaptic inhibition; superfusion of the adult brain stem preparation with artificial CSF containing the glycine-receptor blocker strychnine induced a sudden change in the timing and shape of fictive lung bursts from a sequential, augmenting pattern to a synchronous onset burst with decrementing trajectory.
) lung burst activity interspersed with rhythmic gill output. Although clusters of neural lung activity appeared in premetamorphic larvae, they were more frequently observed in postmetamorphic ventilatory patterns (Fig. 5B) and may be correlated with episodes of uniform lung ventilations or lung inflation cycles described in intact adult frogs (DeJongh and Gans 1969; Kogo et al. 1994a,b). This pattern agrees with previous descriptions of postmetamorphic tadpole ventilation in both the isolated brain stem preparation (Torgerson et al. 1997a) and intact, freely swimming animal (Burggren and Doyle 1986; Infantino 1992; West and Burggren 1982).
,b), whereas in the adult frog oropharyngeal cavity ventilation is performed by activation of elevator and depressors muscles innervated by branches of CN V and SN II (Sakakibara 1984a,b). The emergence of gill motor output in SN II of postmetamorphic larvae corresponds with spontaneous oropharyngeal bursting in specific branches of SN II observed in the in vitro adult frog brain stem preparation (Kogo et al. 1994a,b; McLean et al. 1995a,b), demonstrating that, as metamorphosis proceeds, the pattern of gill motor output takes on adult characteristics.
,b), and Kimura et al. (1997) in the adult frog, demonstrating similarity between postmetamorphic and adult lung ventilatory cycles.
| |
ACKNOWLEDGEMENTS |
|---|
This work was supported by the Alberta Heritage Foundation for Medical Research and the Medical Research Council of Canada.
| |
FOOTNOTES |
|---|
Address for reprint requests: J. E. Remmers, Faculty of Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta T2N 4N1, Canada.
Received 7 October 1997; accepted in final form 8 June 1998.
| |
REFERENCES |
|---|
|
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
RegulationEvolution. Amsterdam: Elsevier, 1988.This article has been cited by other articles:
|
|
 |
|
  S. Fournier, M. Allard, S. Roussin, and R. Kinkead Developmental changes in central O2 chemoreflex in Rana catesbeiana: the role of noradrenergic modulation J. Exp. Biol., September 1, 2007; 210(17): 3015 - 3026. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. Belzile, R. Gulemetova, and R. Kinkead Effects of medullary Raphe stimulation on fictive lung ventilation during development in Rana catesbeiana J. Exp. Biol., June 15, 2007; 210(12): 2046 - 2056. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Fournier and R. Kinkead Noradrenergic modulation of respiratory motor output during tadpole development: role of {alpha}-adrenoceptors J. Exp. Biol., September 15, 2006; 209(18): 3685 - 3694. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. E. Winmill, A. K. Chen, and M. S. Hedrick Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrog Rana catesbeiana J. Exp. Biol., January 15, 2005; 208(2): 213 - 222. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Kinkead, O. Belzile, and R. Gulemetova Serotonergic modulation of respiratory motor output during tadpole development J Appl Physiol, September 1, 2002; 93(3): 936 - 946. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. B. Harris, R. J. A. Wilson, K. Vasilakos, B. E. Taylor, and J. E. Remmers Central respiratory activity of the tadpole in vitro brain stem is modulated diversely by nitric oxide Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2002; 283(2): R417 - R428. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Broch, R. D. Morales, A. V. Sandoval, and M. S. Hedrick Regulation of the respiratory central pattern generator by chloride-dependent inhibition during development in the bullfrog (Rana catesbeiana) J. Exp. Biol., April 15, 2002; 205(8): 1161 - 1169. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Torgerson, M. J. Gdovin, and J. E. Remmers Sites of respiratory rhythmogenesis during development in the tadpole Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2001; 280(4): R913 - R920. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Torgerson, M. J. Gdovin, R. Brandt, and J. E. Remmers Location of central respiratory chemoreceptors in the developing tadpole Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2001; 280(4): R921 - R928. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. J. A. Wilson, K. Vasilakos, M. B. Harris, C. Straus, and J. E. Remmers Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators J. Physiol., April 15, 2002; 540(2): 557 - 570. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
