Postnatal changes in cytochrome oxidase expressions in brain stem nuclei of rats: implications for sensitive periods

2003 ◽  
Vol 95 (6) ◽  
pp. 2285-2291 ◽  
Author(s):  
Qiuli Liu ◽  
Margaret T. T. Wong-Riley

Previously, we reported that cytochrome oxidase (CO) activity in the rat pre-Bötzinger complex (PBC) exhibited a plateau on postnatal days (P) 3–4 and a prominent decrease on P12 (Liu and Wong-Riley, J Appl Physiol 92: 923–934, 2002). These changes were correlated with a concomitant reduction in the expression of glutamate and N-methyl-d-aspartate receptor subunit 1 and an increase in GABA, GABAB, glycine receptor, and glutamate receptor 2. To determine whether changes were limited to the PBC, the present study aimed at examining the expression of CO in a number of brain stem nuclei, with or without known respiratory functions from P0 to P21 in rats: the ventrolateral subnucleus of the solitary tract nucleus, nucleus ambiguus, hypoglossal nucleus, nucleus raphe obscurus, dorsal motor nucleus of the vagus nerve, medial accessory olivary nucleus, spinal nucleus of the trigeminal nerve, and medial vestibular nucleus (MVe). Results indicated that, in all of the brain stem nuclei examined, CO activity exhibited a general increase with age from P0 to P21, with MVe having the slowest rise. Notably, in all of the nuclei examined except for MVe, there was a plateau or decrease at P3–P4 and a prominent rise-fall-rise pattern at P11–P13, similar to that observed in the PBC. In addition, there was a fall-rise-fall pattern at P15–P17 in these nuclei, instead of a plateau pattern in the PBC. Our data suggest that the two postnatal periods with reduced CO activity, P3–P4 and especially P12, may represent common sensitive periods for most of the brain stem nuclei with known or suspected respiratory control functions.

2005 ◽  
Vol 98 (4) ◽  
pp. 1442-1457 ◽  
Author(s):  
Qiuli Liu ◽  
Margaret T. T. Wong-Riley

Previously, we reported that the expression of cytochrome oxidase in a number of brain stem nuclei exhibited a plateau or reduction at postnatal day (P) 3–4 and a dramatic decrease at P12, against a general increase with age. The present study examined the expression of glutamate, N-methyl-d-aspartate receptor subunit 1 (NMDAR1), GABA, GABAB receptors, glycine receptors, and glutamate receptor subunit 2 (GluR2) in the ventrolateral subnucleus of the solitary tract nucleus, nucleus ambiguus, hypoglossal nucleus, medial accessory olivary nucleus, dorsal motor nucleus of the vagus, and cuneate nucleus, from P2 to P21 in rats. Results showed that 1) the expression of glutamate increased with age in a majority of the nuclei, whereas that of NMDAR1 showed heterogeneity among the nuclei; 2) GABA and GABAB expressions decreased with age, whereas that of glycine receptors increased with age; 3) GluR2 showed two peaks, at P3–4 and P12; and 4) glutamate and NMDAR1 showed a significant reduction, whereas GABA, GABAB receptors, glycine receptors, and GluR2 exhibited a concomitant increase at P12. These features were present but less pronounced in hypoglossal nucleus and dorsal motor nucleus of the vagus and were absent in the cuneate nucleus. These data suggest that brain stem nuclei, directly or indirectly related to respiratory control, share a common developmental trend with the pre-Bötzinger complex in having a transient period of imbalance between inhibitory and excitatory drives at P12. During this critical period, the respiratory system may be more vulnerable to excessive exogenous stressors.


2004 ◽  
Vol 286 (4) ◽  
pp. R625-R633 ◽  
Author(s):  
Zixi (Jack) Cheng ◽  
Hong Zhang ◽  
Shang Z. Guo ◽  
Robert Wurster ◽  
David Gozal

In previous single-labeling experiments, we showed that neurons in the nucleus ambiguus (NA) and the dorsal motor nucleus of the vagus (DmnX) project to intrinsic cardiac ganglia. Neurons in these two motor nuclei differ significantly in the size of their projection fields, axon caliber, and endings in cardiac ganglia. These differences in NA and DmnX axon cardiac projections raise the question as to whether they target the same, distinct, or overlapping populations of cardiac principal neurons. To address this issue, we examined vagal terminals in cardiac ganglia and tracer injection sites in the brain stem using two different anterograde tracers {1,1′-dioleyl-3,3,3′,3′-tetramethylindocarbocyanine methanesulfonate and 4-[4-(dihexadecylamino)-styryl]- N-methylpyridinium iodide} and confocal microscopy in male Sprague-Dawley rats. We found that 1) NA and DmnX neurons innervate the same cardiac ganglia, but these axons target separate subpopulations of principal neurons and 2) axons arising from neurons in the NA and DmnX in the contralateral sides of the brain stem enter the cardiac ganglionic plexus through separate bundles and preferentially innervate principal neurons near their entry regions, providing topographic mapping of vagal motor neurons in left and right brain stem vagal nuclei. Because the NA and DmnX project to distinct populations of cardiac principal neurons, we propose that they may play different roles in controlling cardiac function.


2017 ◽  
Vol 117 (1) ◽  
pp. 178-194 ◽  
Author(s):  
Ayako Yamaguchi ◽  
Jessica Cavin Barnes ◽  
Todd Appleby

Central pattern generators (CPGs) in the brain stem are considered to underlie vocalizations in many vertebrate species, but the detailed mechanisms underlying how motor rhythms are generated, coordinated, and initiated remain unclear. We addressed these issues using isolated brain preparations of Xenopus laevis from which fictive vocalizations can be elicited. Advertisement calls of male X. laevis that consist of fast and slow trills are generated by vocal CPGs contained in the brain stem. Brain stem central vocal pathways consist of a premotor nucleus [dorsal tegmental area of medulla (DTAM)] and a laryngeal motor nucleus [a homologue of nucleus ambiguus (n.IX-X)] with extensive reciprocal connections between the nuclei. In addition, DTAM receives descending inputs from the extended amygdala. We found that unilateral transection of the projections between DTAM and n.IX-X eliminated premotor fictive fast trill patterns but did not affect fictive slow trills, suggesting that the fast and slow trill CPGs are distinct; the slow trill CPG is contained in n.IX-X, and the fast trill CPG spans DTAM and n.IX-X. Midline transections that eliminated the anterior, posterior, or both commissures caused no change in the temporal structure of fictive calls, but bilateral synchrony was lost, indicating that the vocal CPGs are contained in the lateral halves of the brain stem and that the commissures synchronize the two oscillators. Furthermore, the elimination of the inputs from extended amygdala to DTAM, in addition to the anterior commissure, resulted in autonomous initiation of fictive fast but not slow trills by each hemibrain stem, indicating that the extended amygdala provides a bilateral signal to initiate fast trills. NEW & NOTEWORTHY Central pattern generators (CPGs) are considered to underlie vocalizations in many vertebrate species, but the detailed mechanisms underlying their functions remain unclear. We addressed this question using an isolated brain preparation of African clawed frogs. We discovered that two vocal phases are mediated by anatomically distinct CPGs, that there are a pair of CPGs contained in the left and right half of the brain stem, and that mechanisms underlying initiation of the two vocal phases are distinct.


1995 ◽  
Vol 109 (1) ◽  
pp. 39-44 ◽  
Author(s):  
Yasumasa Tanaka ◽  
Yoshikazu Yoshida ◽  
Minoru Hirano

AbstractTo demonstrate morphologically the neurons participating in the4aryngeal reflex, Fos-expression, activated with tactile stimulation of the laryngeal vestibulum, was mapped in the cat's lower brain stem utilizing immunohistochemistry. In the stimulation group, many Fos-immunoreactive (ir) neurons were recognized in the nucleus tractus solitarii (NTS) from the level of the most rostral portion of the dorsal motor nucleus of the vagus to the level of the most caudal portion of the inferior olivary nucleus (IO), and in the nucleus ambiguus (NA) from the level of the rostral end of the hypoglossal nucleus to the level of the caudal end of the IO, bilaterally. While some Fos-ir cells were found in the spinal nucleus of the trigeminus, they were also found in the reticular nuclei bilaterally. In the control group, Fos-ir cells were distinctly fewer in number than those in the stimulation group. The results suggested that in the brain stem, the laryngeal reflex pathways have more than two synaptic relays through the interneurons in between the NTS and the NA.


1997 ◽  
Vol 78 (6) ◽  
pp. 3508-3510 ◽  
Author(s):  
Jens C. Rekling ◽  
Jack L. Feldman

Rekling, Jens C. and Jack L. Feldman. Bidirectional electrical coupling between inspiratory motoneurons in the newborn mouse nucleus ambiguus. J. Neurophysiol. 78: 3508–3510, 1997. Some spinal and brain stem motoneurons are electrically coupled in the early postnatal period. To test whether respiratory motoneurons in the brain stem are electrically coupled, we performed single and dual whole cell patch recordings from presumptive motoneurons in the nucleus ambiguus in a rhythmically active brain stem slice from newborn mice. Two of eight (25%) biocytin-injected neurons showed dye-coupling and 4 of 11 (36%) of intracellularly recorded pairs of neurons showed evidence of bidirectional electrical coupling. Impulse activity in one cell elicited small spikelets in the other and hyperpolarization of one cell led to hyperpolarization of the other with a coupling ratio (Δ V 2:Δ V 1) of 0.03–0.14. We conclude that inspiratory ambiguus motoneurons in the newborn mouse brain stem are bidirectionally electrically coupled, which may serve to transmit or coordinate signals, chemical or electrical.


Neuroscience ◽  
2010 ◽  
Vol 170 (1) ◽  
pp. 348-360 ◽  
Author(s):  
A.J. Camp ◽  
R. Lim ◽  
W.B. Anderson ◽  
P.R. Schofield ◽  
R.J. Callister ◽  
...  

1992 ◽  
Vol 262 (5) ◽  
pp. L549-L554 ◽  
Author(s):  
D. F. Donnelly ◽  
C. Jiang ◽  
G. G. Haddad

Most mammalian neurons are known to be sensitive to oxygen availability, but the nature of the sensitivity is not well understood. Previous results have suggested that brain stem neurons may respond differently than cortical neurons during oxygen deprivation. We pursued this hypothesis by examining the time course of change in membrane potential (Vm) and input resistance (Rn) during periods of reduced oxygen availability in a tissue slice preparation. Since extracellular potassium is an important factor determining resting membrane potential, extracellular K+ activity, (K+o), was also measured. Adult rat neurons from three regions were recorded: hippocampal CA1 region, hypoglossal nucleus (XII), and dorsal vagal motor nucleus (DMNX). At the end of a 5-min hypoxic exposure, all neurons depolarized and this depolarization was greatest in XII (28.8 +/- 3.2 mV) compared with DMNX (17.8 +/- 3.7 mV) and CA1 (6.7 +/- 4.4 mV). K+o increased in all regions and was larger in DMNX (7.1 +/- 2.6 mM) and XII (5.3 +/- 2.1 mM) compared with CA1 (2.2 +/- 1.4 mM). During more severe oxygen deprivation (anoxia), neurons also depolarized at different rates with XII greater than DMNX greater than CA1. K+o increased markedly (28–36 mM) by 5 min into anoxia, and no statistical difference was observed between regions. From these results we conclude that 1) all cells tested were depolarized after 5 min of hypoxia; however, regional variability exists in the sensitivity to hypoxia; brain stem neurons depolarize faster than cortical neurons; 2) during anoxia, all brain stem and cortical neurons show a major depolarization, and 3) these differences in membrane potential cannot be solely attributed to changes in extracellular K+.


1996 ◽  
Vol 81 (4) ◽  
pp. 1772-1777 ◽  
Author(s):  
J. C. Lamanna ◽  
M. A. Haxhiu ◽  
K. L. Kutina-Nelson ◽  
S. Pundik ◽  
B. Erokwu ◽  
...  

LaManna, J. C., M. A. Haxhiu, K. L. Kutina-Nelson, S. Pundik, B. Erokwu, E. R. Yeh, W. D. Lust, and N. S. Cherniack.Decreased energy metabolism in brain stem during central respiratory depression in response to hypoxia. J. Appl. Physiol. 81(4): 1772–1777, 1996.—Metabolic changes in the brain stem were measured at the time when oxygen deprivation-induced respiratory depression occurred. Eucapnic ventilation with 8% oxygen in vagotomized urethan-anesthetized rats resulted in cessation of respiratory drive, monitored by recording diaphragm electromyographic activity, on average within 11 min (range 5–27 min), presumably via central depressant mechanisms. At that time, the brain stems were frozen in situ for metabolic analyses. By using 20-μm lyophilized sections from frozen-fixed brain stem, microregional analyses of ATP, phosphocreatine, lactate, and intracellular pH were made from 1) the ventral portion of the nucleus gigantocellularis and the parapyramidal nucleus; 2) the compact and ventral portions of the nucleus ambiguus; 3) midline neurons; 4) nucleus tractus solitarii; and 5) the spinal trigeminal nucleus. At the time of respiratory depression, lactate was elevated threefold in all regions. Both ATP and phosphocreatine were decreased to 50 and 25% of control, respectively. Intracellular pH was more acidic by 0.2–0.4 unit in these regions but was relatively preserved in the chemosensitive regions near the ventral and dorsal medullary surfaces. These results show that hypoxia-induced respiratory depression was accompanied by metabolic changes within brain stem regions involved in respiratory and cardiovascular control. Thus it appears that there was significant energy deficiency in the brain stem after hypoxia-induced respiratory depression had occurred.


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