title: Stimulation of the midbrain periaqueductal gray modulates preinspiratory neurons in the ventrolateral medulla in the rat in vivo.
abstract: The midbrain periaqueductal gray (PAG) is involved in many basic survival behaviors that affect respiration. We hypothesized that the PAG promotes these behaviors by changing the firing of preinspiratory (pre-I) neurons in the pre-Bötzinger complex, a cell group thought to be important in generating respiratory rhythm. We tested this hypothesis by recording single unit activity of pre-Bötzinger pre-I neurons during stimulation in different parts of the PAG. Stimulation in the dorsal PAG increased the firing of pre-I neurons, resulting in tachypnea. Stimulation in the medial part of the lateral PAG converted the pre-I neurons into inspiratory phase-spanning cells, resulting in inspiratory apneusis. Stimulation in the lateral part of the lateral PAG generated an early onset of the pre-I neuronal discharge, which continued throughout the inspiratory phase, while at the same time attenuating diaphragm contraction. Stimulation in the ventral part of the lateral PAG induced tachypnea but inhibited pre-I cell firing, whereas stimulation in the ventrolateral PAG inhibited not only pre-I cells but also the diaphragm, leading to apnea. These findings show that PAG stimulation changes the activity of the pre-Bötzinger pre-I neurons. These changes are in line with the different behaviors generated by the PAG, such as the dorsal PAG generating avoidance behavior, the lateral PAG generating fight and flight, and the ventrolateral PAG generating freezing and immobility.
authors: The University of Queensland Centre for Clinical Research, Herston, Queensland, 4029, Australia.
authors: Hari H
authors: HH
authors: Subramanian
authors: Gert
authors: G
authors: Holstege
mesh_terms: D000200:Action Potentials / Q000187:drug effects; D000704:Analysis of Variance; D000818:Animals; D004576:Electromyography; D005583:Fourier Analysis; D007839:Functional Laterality; D006710:Homocysteine / Q000031:analogs & derivatives / Q000494:pharmacology; D008297:Male; D008526:Medulla Oblongata / Q000166:cytology* / Q000502:physiology; D009434:Neural Pathways / Q000187:drug effects / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D010487:Periaqueductal Gray / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D012119:Respiration
chemical_list: D006710:Homocysteine; C007956:homocysteic acid
keywords: inspiration; periaqueductal gray; pre-Bötzinger; pre-I neuron; respiration; emotional behavior
references: J Comp Neurol. 2010 May 15;518(10):1862-78
references: 20235095
references: Science. 1972 Jul 28;177(4046):364-6
references: 5064328
references: Auton Neurosci. 2007 Jul 31;134(1-2):45-54
references: 17363338
references: J Physiol. 1996 Jun 15;493 ( Pt 3):819-31
references: 8799902
references: Prog Neurobiol. 1995 Aug;46(6):575-605
references: 8545545
references: Brain Res. 1990 Jun 18;520(1-2):73-82
references: 2207648
references: Trends Neurosci. 2001 Aug;24(8):464-72
references: 11476886
references: Nat New Biol. 1971 Feb 17;229(7):222-3
references: 5281024
references: J Neurophysiol. 2011 Jun;105(6):2852-62
references: 21451058
references: J Neurosci. 2000 Dec 1;20(23):RC113
references: 11090613
references: Curr Opin Neurobiol. 1996 Dec;6(6):817-25
references: 9000025
references: Brain Res. 1998 Nov 2;809(2):204-13
references: 9853112
references: J Neural Transm. 1974;35(4):327-35
references: 4436672
references: Pacing Clin Electrophysiol. 1987 Jan;10(1 Pt 2):213-6
references: 2436181
references: Adv Exp Med Biol. 2010;669:353-8
references: 20217381
references: J Physiol. 2009 Oct 15;587(Pt 20):4931-48
references: 19703965
references: J Physiol. 2011 Apr 15;589(Pt 8):2065-78
references: 21486804
references: J Neurophysiol. 1994 Dec;72(6):2598-608
references: 7897477
references: J Physiol. 2013 Jan 1;591(1):109-22
references: 23129795
references: Pflugers Arch. 1987 Nov;410(4-5):420-7
references: 3432049
references: Brain Res. 1988 Jan 26;439(1-2):95-106
references: 3359200
references: Trends Neurosci. 2013 Mar;36(3):152-62
references: 23254296
references: Philos Trans R Soc Lond B Biol Sci. 2009 Sep 12;364(1529):2577-87
references: 19651658
references: Annu Rev Physiol. 2013;75:423-52
references: 23121137
references: J Physiol. 2003 May 1;548(Pt 3):859-74
references: 12640009
references: Brain Res. 1970 Nov 11;24(1):11-28
references: 5503233
references: Respir Physiol. 2000 May;120(3):185-95
references: 10828337
references: Eur J Morphol. 1992;30(1):67-79
references: 1642954
references: Behav Brain Res. 1993 Dec 20;58(1-2):27-47
references: 8136048
references: Neuroscience. 2012 Jan 3;200:59-73
references: 22062132
references: J Neurosci Methods. 1982 Nov;6(4):351-63
references: 6130191
references: Nat Neurosci. 2001 Sep;4(9):927-30
references: 11528424
references: J Neurophysiol. 2001 Jul;86(1):438-46
references: 11431523
references: Nature. 1999 Jul 22;400(6742):360-3
references: 10432113
references: J Neurophysiol. 1995 Apr;73(4):1452-61
references: 7643160
references: Neurosurgery. 2012 Feb;70(2):469-77; discussion 477-8
references: 21841525
references: J Appl Physiol (1985). 2004 Mar;96(3):1146-54
references: 14594859
references: J Neurophysiol. 1994 Sep;72(3):1337-56
references: 7807216
references: Neuroimage. 2012 Mar;60(1):505-22
references: 22197740
references: Nat Neurosci. 2006 Mar;9(3):311-3
references: 16474390
references: Neural Plast. 2009;2009:108135
references: 19283082
references: J Comp Neurol. 1989 Jun 8;284(2):242-52
references: 2754035
references: Respir Physiol Neurobiol. 2008 Dec 10;164(1-2):3-11
references: 18706532
references: J Neurosurg. 1969 Jan;30(1):14-24
references: 4885810
references: J Comp Neurol. 1994 Sep 1;347(1):64-86
references: 7798382
references: Science. 1991 Nov 1;254(5032):726-9
references: 1683005
references: J Neurosci. 2008 Nov 19;28(47):12274-83
references: 19020021
references: J Exp Biol. 1982 Oct;100:93-107
references: 6757372
references: J Physiol. 2009 Nov 1;587(Pt 21):5149-62
references: 19752114
references: Exp Brain Res. 1974;21(4):441-5
references: 4442496
references: Am J Physiol Regul Integr Comp Physiol. 2010 Sep;299(3):R853-61
references: 20504909
references: J Neurosci. 2009 Mar 25;29(12):3824-32
references: 19321779
references: Respir Physiol Neurobiol. 2008 Dec 10;164(1-2):96-104
references: 18602029
references: Nat Rev Neurosci. 2006 Mar;7(3):232-42
references: 16495944
references: Philos Trans R Soc Lond B Biol Sci. 2009 Sep 12;364(1529):2625-33
references: 19651662
references: Neurourol Urodyn. 2010;29(1):42-8
references: 20025036