Cell–cell coupling occurs in dorsal medullary neurons after minimizing anatomical-coupling artifacts

Dean, J. Michael; Huang, Ren-Qi; Erlichman, Joseph S.; Southard, Teresa; Hellard, David

doi:10.1016/s0306-4522(97)00016-x

Cited by 51 publications

(34 citation statements)

References 63 publications

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“…Chemosensitive neurons have been claimed to be intrinsic based on the elimination of vesicular chemical neurotransmitter release (7,24,32,40) using either high Mg 2ϩ /low Ca 2ϩ solutions or receptor-blocking cocktails. More recent evidence shows that gap junctions are expressed in neurons from chemosensitive regions (9,46,48) and are preferentially expressed in CO 2 -sensitive neurons from the NTS (8,18). We have thus recently (5), and in the current study, extended the definition of an intrinsically chemosensitive neuron to one that still responds to hypercapnia when both vesicular chemical neurotransmitter release and electrical synaptic activity are blocked.…”

Section: Discussionmentioning

confidence: 61%

“…The blind whole cell patch-clamp technique was used to measure neuronal membrane potential (V m) and integrated firing rate, as described previously (1). The experimental setup that was used has been previously described (5,8,14,18). Briefly, a whole cell patch pipette (5 M⍀) was fabricated from borosilicate glass using a Narishige PP-830 dual-stage pipette puller.…”

Section: Solutionsmentioning

confidence: 99%

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Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Nichols¹,

Mulkey²,

Wilkinson³

et al. 2009

American Journal of Physiology-Regulatory, Integrative and Comp

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(pH i) and electrical responses to hypercapnic acidosis (HA). SC neurons were recorded using the blind whole cell patchclamp technique and loading the soma with the pH-sensitive dye pyranine through the patch pipette. We found that SC neurons from adult rats have a lower steady-state pH i than SC neurons from neonatal rats. In the presence of chemical and electrical synaptic blockade, adult SC neurons have firing rate responses to HA (percentage of neurons activated or inhibited and the magnitude of response as determined by the chemosensitivity index) that are similar to SC neurons from neonatal rats. They also have a typical response to isohydric hypercapnia, including decreased ⌬pHi, followed by pHi recovery, and increased firing rate. Thus, the chemosensitive response of SC neurons from adults is similar to the chemosensitive response of SC neurons from neonatal rats. Because our findings for adults are similar to previously reported values for neurons from neonatal rats, we conclude that intrinsic chemosensitivity is established early in development for SC neurons and is maintained throughout adulthood.

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Section: Discussionmentioning

confidence: 61%

Section: Solutionsmentioning

confidence: 99%

Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Nichols¹,

Mulkey²,

Wilkinson³

et al. 2009

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Once detected, the neurons' position was confirmed under bright field illumination using DIC (Nomarski) optics. Whole cell recordings were performed with patch pipettes (3)(4)(5)(6)(7)(8) filled with a potassium gluconate intracellular solution (in mM: K-gluconate 128, 10 KCl, 0.3 CaCl 2 , 1 MgCl 2 , 10 Hepes, 1 EGTA, 2 ATP, 0.25 GTP adjusted to pH 7.35 with KOH) using a single-electrode voltage clamp amplifier (Axoclamp 2B, Axon Instr., Union City, CA). Data were filtered at 2 kHz, digitized via a Digidata 1320 interface (Axon Instr.…”

Section: Methodsmentioning

confidence: 99%

“…The majority of the in vitro experimental investigations, however, have been conducted on coronal brainstem slices [5][6][7]20,22,23,25].…”

Section: Introductionmentioning

confidence: 99%

Morphological differences between planes of section do not influence the electrophysiological properties of identified rat dorsal motor nucleus of the vagus neurons

2004

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Recent cytoarchitectonic studies have shown that the dorsal motor nucleus of the vagus (DMV) comprises neurons with different morphological features. Our own studies, conducted in horizontal brainstem slices, have shown that DMV neurons projecting to stomach areas can be distinguished from neurons projecting to the intestine on the basis of their electrophysiological as well as morphological properties. The majority of the in vitro experimental investigations, however, have been conducted on coronal brainstem slices. The aim of the present study was to assess whether the electrophysiological properties of DMV neurons are due to intrinsic membrane properties of the neurons or are dependent upon the plane of section, i.e., coronal vs. horizontal, in which the brainstem is cut. The fluorescent retrograde tracer DiI was applied to either the stomach or intestine of rats. Whole cell recordings were subsequently made from labeled DMV neurons in thin brainstem slices sectioned in either the horizontal or coronal plane. In the horizontal plane, both the somata and the dendritic tree of gastric-projecting neurons were smaller than intestinalprojecting neurons. In the coronal plane, however, apart from a smaller soma diameter in gastricprojecting neurons, morphological differences were not found between the groups. The electrophysiological differences observed between the groups were, however, consistent in both planes of section, that is, intestinal-projecting neurons had larger and longer afterhyperpolarization (AHP) as well as slower frequency-responses to depolarizing stimuli than gastric-projecting neurons. Our data suggest that intrinsic rather than morphological features govern the electrophysiological characteristics of DMV neurons.

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“…When using hypercapnic stimuli without a change of extracellular pH (pH o ), an increase in spike frequency without an apparent membrane depolarization has been observed in both LC (26) and medullary raphe neurons (62). Furthermore, an increase in membrane input resistance, which should be associated with K ϩ channel closure in response to chemosensitive signals, is often very small (18,42), suggesting that multiple channels may be affected, with some closing and others opening. Indeed, Richerson (43) suggested the possibility of several chemosensitive channels being affected by chemosensitive signals in concert.…”

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confidence: 99%

Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K⁺ and Ca²⁺channels

Filosa

Putnam

2003

American Journal of Physiology-Cell Physiology

113

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Filosa, Jessica A., and Robert W. Putnam. Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K ϩ and Ca 2ϩ channels. Am J Physiol Cell Physiol 284: C145-C155, 2003. First published September 18, 2002 10.1152/ajpcell.00346.2002We studied chemosensitive signaling in locus coeruleus (LC) neurons using both perforated and whole cell patch techniques. Upon inhibition of fast Na ϩ spikes by tetrodotoxin (TTX), hypercapnic acidosis [HA; 15% CO 2, extracellular pH (pHo) 6.8] induced small, slow spikes. These spikes were inhibited by Co 2ϩ or nifedipine and were attributed to activation of L-type Ca 2ϩ channels by HA. Upon inhibition of both Na ϩ and Ca 2ϩ spikes, HA resulted in a membrane depolarization of 3.52 Ϯ 0.61 mV (n ϭ 17) that was reduced by tetraethylammonium (TEA) (1.49 Ϯ 0.70 mV, n ϭ 7; P Ͻ 0.05) and absent (Ϫ0.97 Ϯ 0.73 mV, n ϭ 7; P Ͻ 0.001) upon exposure to isohydric hypercapnia (IH; 15% CO2, 77 mM HCO 3 Ϫ , pHo 7.45). Either HA or IH, but not 50 mM Na-propionate, activated Ca 2ϩ channels. Inhibition of L-type Ca 2ϩ channels by nifedipine reduced HA-induced increased firing rate and eliminated IH-induced increased firing rate. We conclude that chemosensitive signals (e.g., HA or IH) have multiple targets in LC neurons, including TEA-sensitive K ϩ channels and TWIKrelated acid-sensitive K ϩ (TASK) channels. Furthermore, HA and IH activate L-type Ca 2ϩ channels, and this activation is part of chemosensitive signaling in LC neurons. acidosis; membrane potential; perforated patch clamp; respiration; whole cell patch clamp CENTRAL CHEMORECEPTION is fundamental for the understanding of cardiovascular and respiratory regulation. A number of different brain stem areas, including the ventrolateral medulla (VLM) (44,45,53), the nucleus tractus solitarii (NTS) (15,19), the rostral medullary raphe (33, 62), and the locus coeruleus (LC) (4, 35), have been shown to contain neurons that are sensitive to chemosensitive stimuli such as high CO 2 /H ϩ or hypercapnic acidosis (HA). These neurons share the common characteristic of, upon an acid challenge, increasing Na ϩ spike frequency. This is particularly true for the LC, in which Ͼ80% of neurons are found to be chemosensitive (26,36), making the LC an ideal nucleus for the study of the cellular basis of chemosensitivity.The current model of cellular chemosensitivity, based on chemosensitive cells located both in the brain stem and the carotid bodies, is that a chemosensitive signal such as high CO 2 /H ϩ results in a neuronal membrane depolarization, presumably through inhibition of a K ϩ channel, resulting in an increased spike frequency (17,35,36,42,63,64). A number of findings suggest that this model may be simplistic. When using hypercapnic stimuli without a change of extracellular pH (pH o ), an increase in spike frequency without an apparent membrane depolarization has been observed in both LC (26) and medullary raphe neurons (62). Furthermore, an increase in membrane input resistance, which should be associated with K ϩ channel closure...

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Cell–cell coupling occurs in dorsal medullary neurons after minimizing anatomical-coupling artifacts

Cited by 51 publications

References 63 publications

Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Morphological differences between planes of section do not influence the electrophysiological properties of identified rat dorsal motor nucleus of the vagus neurons

Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K⁺ and Ca²⁺channels

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Cell–cell coupling occurs in dorsal medullary neurons after minimizing anatomical-coupling artifacts

Cited by 51 publications

References 63 publications

Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Characterization of the chemosensitive response of individual solitary complex neurons from adult rats

Morphological differences between planes of section do not influence the electrophysiological properties of identified rat dorsal motor nucleus of the vagus neurons

Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K+ and Ca2+channels

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Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K⁺ and Ca²⁺channels