Abstract
We visualized respiratory neuron activity covering the entire ventral medulla using optical recordings in a newborn rat brainstem-spinal cord preparation stained with voltage-sensitive dye. We measured optical signals from several seconds before to several seconds after the inspiratory phase using the inspiratory motor nerve discharge as the trigger signal; we averaged the optical signals of 50-150 respiratory cycles to obtain an optical image correlating particularly to inspiratory activity. The optical images we obtained from the ventral approach indicated that neuron activity first appeared during the respiratory cycle in the limited region of the rostral ventrolateral medulla (RVLM), preceding the onset of inspiratory activity by approximately 500 msec. During the inspiratory phase, plateau activity appeared in the more caudal ventrolateral medulla at the level of the most rostral roots of the XIIth nerve. Comparison with electrophysiological recordings from respiratory neurons in the RVLM suggested that the optical signals preceding the inspiratory burst reflect preinspiratory neuron activity in this area. This RVLM area was determined to be ventrolateral to the facial nucleus and close to the ventral surface. We referred to this functional neuron group as the para-facial respiratory group (pFRG). Partial, bilateral electrical lesioning of the pFRG significantly reduced the respiratory frequency, together with changes in the spatiotemporal pattern of respiratory neuron activity. Our findings suggest that the pFRG comprises a neuronal population that is involved in the primary respiratory rhythm generation in the rostrocaudally extending respiratory neuron network of the medulla.
MeSH Terms
Animals
Animals, Newborn
Culture Techniques
Fluorescent Dyes
Kinetics
Medulla Oblongata/cytology,physiology
Microscopy, Fluorescence
Neurons/cytology,physiology
Patch-Clamp Techniques
Periodicity
Pyridinium Compounds
Rats
Rats, Wistar
Respiration
Chemicals
Fluorescent Dyes
Pyridinium Compounds
1-(3-sulfonatopropyl)-4-(beta)(2-(di-n-butylamino)-6-naphthylvinyl)pyridinium betaine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Onimaru Hiroshi
Showa University School of Medicine, Shinagawa-ku, Tokyo 142-8555, Japan. oni@med.showa-u.ac.jp
Homma Ikuo
References (27)
27 references, click to expand
-
Neuronal pacemaker for breathing visualized in vitro.
Nature. 1999 Jul 22;400(6742):360-3
PMID: 10432113
-
Respiratory network function in the isolated brainstem-spinal cord of newborn rats.
Prog Neurobiol. 1999 Dec;59(6):583-634
PMID: 10845755
-
Quantification of optical signals with electrophysiological signals in neural activities of Di-4-ANEPPS stained rat hippocampal slices.
J Neurosci Methods. 2000 Oct 15;102(1):11-23
PMID: 11000407
-
Possible role of retrotrapezoid nucleus and parapyramidal area in the respiratory response to anoxia: an in vitro study in neonatal rat.
Neurosci Lett. 2000 Dec 1;295(1-2):67-9
PMID: 11078938
-
Optical approaches to embryonic development of neural functions in the brainstem.
Prog Neurobiol. 2001 Feb;63(2):151-97
PMID: 11124445
-
Models of respiratory rhythm generation in the pre-Bötzinger complex. III. Experimental tests of model predictions.
J Neurophysiol. 2001 Jul;86(1):59-74
PMID: 11431488
-
Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models.
Trends Neurosci. 2001 Aug;24(8):464-72
PMID: 11476886
-
Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons.
Nat Neurosci. 2001 Sep;4(9):927-30
PMID: 11528424
-
Optical recording of spontaneous respiratory neuron activity in the rat brain stem.
Jpn J Physiol. 2001 Oct;51(5):613-9
PMID: 11734083
-
Central chemosensitivity, sleep, and wakefulness.
Respir Physiol. 2001 Dec;129(1-2):257-68
PMID: 11738659
-
Whole cell recordings from respiratory neurons in the medulla of brainstem-spinal cord preparations isolated from newborn rats.
Pflugers Arch. 1992 Mar;420(3-4):399-406
PMID: 1598195
-
Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals.
Science. 1991 Nov 1;254(5032):726-9
PMID: 1683005
-
Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity.
J Neurophysiol. 1990 Oct;64(4):1149-69
PMID: 2258739
-
Respiratory activity in retrotrapezoid nucleus in cat.
Am J Physiol. 1990 Feb;258(2 Pt 1):L33-44
PMID: 2305898
-
Brainstem connections of the rostral ventral respiratory group of the rat.
Brain Res. 1990 Apr 9;513(1):35-42
PMID: 2350683
-
Respiration-related neurons in the ventral medulla of newborn rats in vitro.
Brain Res Bull. 1990 Apr;24(4):599-604
PMID: 2357591
-
Brainstem projections to the major respiratory neuron populations in the medulla of the cat.
J Comp Neurol. 1989 Mar 1;281(1):69-96
PMID: 2466879
-
Retrotrapezoid nucleus in the rat.
Neurosci Lett. 1989 Jun 19;101(2):138-42
PMID: 2771161
-
Optical imaging of neuronal activity.
Physiol Rev. 1988 Oct;68(4):1285-366
PMID: 3054949
-
Primary respiratory rhythm generator in the medulla of brainstem-spinal cord preparation from newborn rat.
Brain Res. 1988 Apr 5;445(2):314-24
PMID: 3370466
-
Optical monitoring of membrane potential: methods of multisite optical measurement.
Soc Gen Physiol Ser. 1986;40:71-99
PMID: 3520842
-
Localization of respiratory rhythm-generating neurons in the medulla of brainstem-spinal cord preparations from newborn rats.
Neurosci Lett. 1987 Jul 22;78(2):151-5
PMID: 3627556
-
Respiratory rhythm generation in the in vitro brain stem-spinal cord preparation of the neonatal rat.
J Physiol. 1984 Sep;354:173-83
PMID: 6148410
-
Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters.
Physiol Rev. 1995 Jan;75(1):1-45
PMID: 7831394
-
Respiratory motor output of the sectioned medulla of the neonatal rat.
Respir Physiol. 1994 Apr;96(1):49-60
PMID: 8023020
-
Brainstem connections of the rat ventral respiratory subgroups: afferent projections.
J Auton Nerv Syst. 1993 Feb;42(2):99-118
PMID: 8383713
-
PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation.
Annu Rev Physiol. 1998;60:385-405
PMID: 9558470