Gamma band unit activity and population responses in the pedunculopontine nucleus.
The pedunculopontine nucleus (PPN) is involved in the activated states of waking and paradoxical sleep, forming part of the reticular activating system (RAS). The studies described tested the hypothesis that single unit and/or population responses of PPN neurons are capable of generating gamma band frequency activity. Whole cell patch clamp recordings (immersion chamber) and population responses (interface chamber) were conducted on 9- to 20-day-old rat brain stem slices. Regardless of cell type (I, II, or III) or type of response to the nonselective cholinergic receptor agonist carbachol (excitation, inhibition, biphasic), almost all PPN neurons fired at gamma band frequency, but no higher, when subjected to depolarizing steps (50 +/- 2 Hz, mean +/- SE). Nonaccommodating neurons fired at 18-100 Hz throughout depolarizing steps, while most accommodating neurons exhibited gamma band frequency of action potentials followed by gamma band membrane oscillations. These oscillations were blocked by the sodium channel blocker tetrodotoxin (TTX), suggesting that at least some are mediated by sodium currents. Population responses in the PPN showed that carbachol induced peaks of activation in the theta and gamma range, while glutamatergic receptor agonists induced overall increases in activity at theta and gamma frequencies, although in differing patterns. Gamma band activity appears to be a part of the intrinsic membrane properties of PPN neurons, and the population as a whole generates different patterns of gamma band activity under the influence of specific transmitters. Given sufficient excitation, the PPN may impart gamma band activation on its targets.
Simon
Christen
C
Center for Translational Neuroscience, Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205, USA.
Kezunovic
Nebojsa
N
Ye
Meijun
M
Hyde
James
J
Hayar
A
A
Williams
D K
DK
Garcia-Rill
E
E
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002217:Carbachol / Q000494:pharmacology; D004569:Electroencephalography / Q000187:drug effects*; D055724:Electrophysiological Phenomena; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D005260:Female; D007608:Kainic Acid / Q000494:pharmacology; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology; D018721:Muscarinic Agonists / Q000494:pharmacology; D016202:N-Methylaspartate / Q000494:pharmacology; D009474:Neurons / Q000187:drug effects / Q000502:physiology; D018408:Patch-Clamp Techniques; D045042:Pedunculopontine Tegmental Nucleus / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D026902:Potassium Channel Blockers / Q000494:pharmacology; D015221:Potassium Channels / Q000502:physiology; D011247:Pregnancy; D051381:Rats; D017207:Rats, Sprague-Dawley; D026941:Sodium Channel Blockers / Q000494:pharmacology; D013779:Tetrodotoxin / Q000494:pharmacology; D013826:Theta Rhythm / Q000187:drug effects
D018690:Excitatory Amino Acid Agonists; D018721:Muscarinic Agonists; D026902:Potassium Channel Blockers; D015221:Potassium Channels; D026941:Sodium Channel Blockers; D013779:Tetrodotoxin; D016202:N-Methylaspartate; D002217:Carbachol; D007608:Kainic Acid
Proc Natl Acad Sci U S A. 2004 May 4;101(18):7152-7
15103017
Am J Physiol Regul Integr Comp Physiol. 2001 Mar;280(3):R752-9
11171654
Exp Brain Res. 1999 May;126(2):160-74
10369139
Sleep. 2008 May;31(5):673-90
18517037
Cereb Cortex. 1997 Sep;7(6):534-45
9276178
Neuroimage. 2010 Feb 15;49(4):3257-68
19932756
Neuropharmacology. 2003 Jun;44(7):864-72
12726818
Trends Neurosci. 2005 Jun;28(6):325-33
15927689
J Neurophysiol. 2001 Mar;85(3):1235-45
11247992
Brain Res. 1990 Sep 17;527(2):213-23
2253034
Sleep. 2009 Sep;32(9):1191-200
19750924
J Neurosci Methods. 2004 Mar 15;134(1):9-21
15102499
Neuroscience. 1997 Jun;78(3):771-94
9153657
Biol Cybern. 1988;60(2):121-30
3228555
J Physiol. 1997 Aug 1;502 ( Pt 3):591-607
9279811
J Neurophysiol. 1992 Oct;68(4):1359-72
1359028
J Neurophysiol. 2010 May;103(5):2417-32
20181729
Hippocampus. 2000;10(2):187-97
10791841
J Neurosci. 1990 Aug;10(8):2560-79
2201752
J Neurophysiol. 2009 Dec;102(6):3689-97
19846619
Neuron. 2008 Jun 12;58(5):763-74
18549787
Int J Psychophysiol. 2009 Sep;73(3):350-4
19481120
Nature. 1998 Jul 9;394(6689):186-9
9671302
Eur J Neurosci. 2009 Jan;29(2):340-58
19200238
J Neurophysiol. 2002 Apr;87(4):1790-8
11929900
Proc Natl Acad Sci U S A. 1989 Mar;86(5):1698-702
2922407
J Neurosci Res. 2002 Nov 15;70(4):611-21
12404515
Nature. 1999 Nov 4;402(6757):75-9
10573419
Proc Natl Acad Sci U S A. 1991 May 15;88(10):4396-400
2034679
Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):897-901
1992481
J Neurosci Res. 2001 Oct 1;66(1):109-16
11599007
J Neurosci. 1990 Aug;10(8):2541-59
2388079
Sleep. 2007 Nov;30(11):1405-14
18041475
Curr Opin Neurobiol. 1999 Apr;9(2):189-94
10322191
Neuroscience. 2006 Dec;143(3):739-55
17008019
Dev Psychobiol. 1970;2(4):216-39
5527153
J Neurophysiol. 2007 Apr;97(4):3142-7
17215497
Annu Rev Physiol. 1993;55:349-74
8466179