Responses of neurons in the nucleus tractus solitarius to stimulation of heart and lung receptors in the rat

Tina Hines, Glenn M Toney, Steven W. Mifflin

Research output: Contribution to journalArticle

48 Citations (Scopus)

Abstract

To characterize central integration of reflex responses to stimulation of mechanically and chemically sensitive receptors in the heart and lung, male rats (350 to 425 g) were anesthetized (pentobarbital, 50 mg/kg IP) and paralyzed (gallamine triethiodide, 25 mg/kg IV), and then they underwent bilateral sinoaortic denervation. Extracellular activity of neurons in the nucleus tractus solitarius (NTS) was recorded in response to bolus intra- atrial saline (50, 100, 200, or 300 μL) or phenylbiguanide (PBG, 16 μg/kg in 100 μL) administered in random sequence. Changes in mean arterial pressure (MAP), mean right atrial pressure, and right atrial systolic pressure (RASP) were measured as correlates of stimulus intensity, and heart rate (HR) and renal sympathetic nerve activity (RSNA) were used to assess efferent reflex effects of cardiac and pulmonary receptor stimulation. NTS neurons with possible afferent input from stretch and chemically sensitive receptors were identified by an excitatory evoked response to electrical stimulation of the ipsilateral vagus nerve (1 Hz, 500 μA, 1-millisecond duration). Thirty-eight vagus nerve-evoked NTS units with onset latencies of 25.3±0.9 milliseconds displayed excitatory or inhibitory responses to saline or PBG injections or to both interventions. Saline administration elicited volume-dependent transient increases in MAP and RASP, which were followed by reflex decreases in MAP, HR, and RSNA. PBG injections also evoked hypotension, bradycardia, and sympathoinhibition. In contrast to the graded effects of graded saline injections on MAP, right atrial pressure, HR, and RSNA, the mean change in peak NTS cell activity after saline injections did not correlate with the volume injected; rather, the cells responded at one volume threshold and did not alter firing when stimulus intensity (ie, the volume injected) was increased. Although the number of NTS units with firing thresholds at the respective volumes was fairly evenly distributed, the total number of cells responding at any given volume was greater as the volume injected increased. Thus, the graded reflex effects observed during volume expansion may involve recruitment of a progressively greater number of responsive neurons and not graded increases in the discharge frequency of any particular NTS cell. These data indicate a high degree of neural integration in the NTS, which may be critical for the reflex adjustments to stimulation of mechanically and chemically sensitive receptors.

Original languageEnglish (US)
Pages (from-to)1188-1196
Number of pages9
JournalCirculation Research
Volume74
Issue number6
StatePublished - Jun 1994

Fingerprint

Solitary Nucleus
Atrial Pressure
Neurons
Reflex
Lung
Arterial Pressure
Injections
Vagus Nerve
Heart Rate
Kidney
Gallamine Triethiodide
Blood Pressure
Social Adjustment
Denervation
Pentobarbital
Bradycardia
Hypotension
Electric Stimulation
Cell Count

Keywords

  • phenylbiguanide
  • renal sympathetic nerve activity
  • right atrial pressure
  • volume expansion

ASJC Scopus subject areas

  • Physiology
  • Cardiology and Cardiovascular Medicine

Cite this

Responses of neurons in the nucleus tractus solitarius to stimulation of heart and lung receptors in the rat. / Hines, Tina; Toney, Glenn M; Mifflin, Steven W.

In: Circulation Research, Vol. 74, No. 6, 06.1994, p. 1188-1196.

Research output: Contribution to journalArticle

@article{8b57a28a01d846de9a6b4d9c6fcd9160,
title = "Responses of neurons in the nucleus tractus solitarius to stimulation of heart and lung receptors in the rat",
abstract = "To characterize central integration of reflex responses to stimulation of mechanically and chemically sensitive receptors in the heart and lung, male rats (350 to 425 g) were anesthetized (pentobarbital, 50 mg/kg IP) and paralyzed (gallamine triethiodide, 25 mg/kg IV), and then they underwent bilateral sinoaortic denervation. Extracellular activity of neurons in the nucleus tractus solitarius (NTS) was recorded in response to bolus intra- atrial saline (50, 100, 200, or 300 μL) or phenylbiguanide (PBG, 16 μg/kg in 100 μL) administered in random sequence. Changes in mean arterial pressure (MAP), mean right atrial pressure, and right atrial systolic pressure (RASP) were measured as correlates of stimulus intensity, and heart rate (HR) and renal sympathetic nerve activity (RSNA) were used to assess efferent reflex effects of cardiac and pulmonary receptor stimulation. NTS neurons with possible afferent input from stretch and chemically sensitive receptors were identified by an excitatory evoked response to electrical stimulation of the ipsilateral vagus nerve (1 Hz, 500 μA, 1-millisecond duration). Thirty-eight vagus nerve-evoked NTS units with onset latencies of 25.3±0.9 milliseconds displayed excitatory or inhibitory responses to saline or PBG injections or to both interventions. Saline administration elicited volume-dependent transient increases in MAP and RASP, which were followed by reflex decreases in MAP, HR, and RSNA. PBG injections also evoked hypotension, bradycardia, and sympathoinhibition. In contrast to the graded effects of graded saline injections on MAP, right atrial pressure, HR, and RSNA, the mean change in peak NTS cell activity after saline injections did not correlate with the volume injected; rather, the cells responded at one volume threshold and did not alter firing when stimulus intensity (ie, the volume injected) was increased. Although the number of NTS units with firing thresholds at the respective volumes was fairly evenly distributed, the total number of cells responding at any given volume was greater as the volume injected increased. Thus, the graded reflex effects observed during volume expansion may involve recruitment of a progressively greater number of responsive neurons and not graded increases in the discharge frequency of any particular NTS cell. These data indicate a high degree of neural integration in the NTS, which may be critical for the reflex adjustments to stimulation of mechanically and chemically sensitive receptors.",
keywords = "phenylbiguanide, renal sympathetic nerve activity, right atrial pressure, volume expansion",
author = "Tina Hines and Toney, {Glenn M} and Mifflin, {Steven W.}",
year = "1994",
month = "6",
language = "English (US)",
volume = "74",
pages = "1188--1196",
journal = "Circulation Research",
issn = "0009-7330",
publisher = "Lippincott Williams and Wilkins",
number = "6",

}

TY - JOUR

T1 - Responses of neurons in the nucleus tractus solitarius to stimulation of heart and lung receptors in the rat

AU - Hines, Tina

AU - Toney, Glenn M

AU - Mifflin, Steven W.

PY - 1994/6

Y1 - 1994/6

N2 - To characterize central integration of reflex responses to stimulation of mechanically and chemically sensitive receptors in the heart and lung, male rats (350 to 425 g) were anesthetized (pentobarbital, 50 mg/kg IP) and paralyzed (gallamine triethiodide, 25 mg/kg IV), and then they underwent bilateral sinoaortic denervation. Extracellular activity of neurons in the nucleus tractus solitarius (NTS) was recorded in response to bolus intra- atrial saline (50, 100, 200, or 300 μL) or phenylbiguanide (PBG, 16 μg/kg in 100 μL) administered in random sequence. Changes in mean arterial pressure (MAP), mean right atrial pressure, and right atrial systolic pressure (RASP) were measured as correlates of stimulus intensity, and heart rate (HR) and renal sympathetic nerve activity (RSNA) were used to assess efferent reflex effects of cardiac and pulmonary receptor stimulation. NTS neurons with possible afferent input from stretch and chemically sensitive receptors were identified by an excitatory evoked response to electrical stimulation of the ipsilateral vagus nerve (1 Hz, 500 μA, 1-millisecond duration). Thirty-eight vagus nerve-evoked NTS units with onset latencies of 25.3±0.9 milliseconds displayed excitatory or inhibitory responses to saline or PBG injections or to both interventions. Saline administration elicited volume-dependent transient increases in MAP and RASP, which were followed by reflex decreases in MAP, HR, and RSNA. PBG injections also evoked hypotension, bradycardia, and sympathoinhibition. In contrast to the graded effects of graded saline injections on MAP, right atrial pressure, HR, and RSNA, the mean change in peak NTS cell activity after saline injections did not correlate with the volume injected; rather, the cells responded at one volume threshold and did not alter firing when stimulus intensity (ie, the volume injected) was increased. Although the number of NTS units with firing thresholds at the respective volumes was fairly evenly distributed, the total number of cells responding at any given volume was greater as the volume injected increased. Thus, the graded reflex effects observed during volume expansion may involve recruitment of a progressively greater number of responsive neurons and not graded increases in the discharge frequency of any particular NTS cell. These data indicate a high degree of neural integration in the NTS, which may be critical for the reflex adjustments to stimulation of mechanically and chemically sensitive receptors.

AB - To characterize central integration of reflex responses to stimulation of mechanically and chemically sensitive receptors in the heart and lung, male rats (350 to 425 g) were anesthetized (pentobarbital, 50 mg/kg IP) and paralyzed (gallamine triethiodide, 25 mg/kg IV), and then they underwent bilateral sinoaortic denervation. Extracellular activity of neurons in the nucleus tractus solitarius (NTS) was recorded in response to bolus intra- atrial saline (50, 100, 200, or 300 μL) or phenylbiguanide (PBG, 16 μg/kg in 100 μL) administered in random sequence. Changes in mean arterial pressure (MAP), mean right atrial pressure, and right atrial systolic pressure (RASP) were measured as correlates of stimulus intensity, and heart rate (HR) and renal sympathetic nerve activity (RSNA) were used to assess efferent reflex effects of cardiac and pulmonary receptor stimulation. NTS neurons with possible afferent input from stretch and chemically sensitive receptors were identified by an excitatory evoked response to electrical stimulation of the ipsilateral vagus nerve (1 Hz, 500 μA, 1-millisecond duration). Thirty-eight vagus nerve-evoked NTS units with onset latencies of 25.3±0.9 milliseconds displayed excitatory or inhibitory responses to saline or PBG injections or to both interventions. Saline administration elicited volume-dependent transient increases in MAP and RASP, which were followed by reflex decreases in MAP, HR, and RSNA. PBG injections also evoked hypotension, bradycardia, and sympathoinhibition. In contrast to the graded effects of graded saline injections on MAP, right atrial pressure, HR, and RSNA, the mean change in peak NTS cell activity after saline injections did not correlate with the volume injected; rather, the cells responded at one volume threshold and did not alter firing when stimulus intensity (ie, the volume injected) was increased. Although the number of NTS units with firing thresholds at the respective volumes was fairly evenly distributed, the total number of cells responding at any given volume was greater as the volume injected increased. Thus, the graded reflex effects observed during volume expansion may involve recruitment of a progressively greater number of responsive neurons and not graded increases in the discharge frequency of any particular NTS cell. These data indicate a high degree of neural integration in the NTS, which may be critical for the reflex adjustments to stimulation of mechanically and chemically sensitive receptors.

KW - phenylbiguanide

KW - renal sympathetic nerve activity

KW - right atrial pressure

KW - volume expansion

UR - http://www.scopus.com/inward/record.url?scp=0028338751&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0028338751&partnerID=8YFLogxK

M3 - Article

C2 - 8187285

AN - SCOPUS:0028338751

VL - 74

SP - 1188

EP - 1196

JO - Circulation Research

JF - Circulation Research

SN - 0009-7330

IS - 6

ER -