Postinhibitory rebound spikes are modulated by the history of membrane hyperpolarization in the SCN.
The suprachiasmatic nucleus (SCN) of the hypothalamus regulates biological circadian time thereby directly impacting numerous physiological processes. The SCN is composed almost exclusively of gamma-aminobutyric acid (GABA)ergic neurons, many of which synapse with other GABAergic cells in the SCN to exert an inhibitory influence on their postsynaptic targets for most, if not all, phases of the circadian cycle. The overwhelmingly GABAergic nature of the SCN, along with its internal connectivity properties, provide a strong model to examine how inhibitory neurotransmission generates output signals. In the present work we show that hyperpolarizations that range from 5 to 1000 ms elicit rebound spikes in 63% of all SCN neurons tested in voltage-clamp in the SCN of adult rats and hamsters. In current-clamp recordings, hyperpolarizations led to rebound spike formation in all cells; however, low-amplitude or short-duration current injections failed to consistently activate rebound spikes. Increasing the duration of hyperpolarization from 5 to 1000 ms is strongly and positively correlated with enhanced spike probability. Additionally, the magnitude of hyperpolarization exerts a strong influence on both the amplitude of the spike, as revealed by voltage-clamp recordings, and the latency to peak current obtained in either voltage- or current-clamp mode. Our results suggest that SCN neurons may use rebound spikes as one means of producing output signals from a largely interconnected network of GABAergic neurons.
Tremere
Liisa A
LA
CROET, OHSU, Portland, OR, USA.
Pinaud
Raphael
R
Irwin
Robert P
RP
Allen
Charles N
CN
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D006224:Cricetinae; D008012:Lidocaine / Q000378:metabolism; D008297:Male; D008564:Membrane Potentials / Q000502:physiology; D008647:Mesocricetus; D009474:Neurons / Q000166:cytology / Q000502:physiology*; D018408:Patch-Clamp Techniques; D051381:Rats; D017207:Rats, Sprague-Dawley; D013493:Suprachiasmatic Nucleus / Q000166:cytology / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D005680:gamma-Aminobutyric Acid; D008012:Lidocaine
Pflugers Arch. 1993 Oct;425(1-2):109-16
7903809
J Neurophysiol. 2002 Mar;87(3):1348-62
11877509
Brain Res Dev Brain Res. 1995 May 26;86(1-2):187-202
7656412
Neuroscience. 2004;123(1):87-99
14667444
Vis Neurosci. 2007 Sep-Oct;24(5):709-31
17908349
J Neurophysiol. 2002 Nov;88(5):2821-33
12424315
J Neurosci. 2003 Feb 15;23(4):1441-50
12598633
Neurosci Lett. 1993 Feb 5;150(1):112-6
8097023
Proc Natl Acad Sci U S A. 1972 Jun;69(6):1583-6
4556464
J Biol Rhythms. 1999 Apr;14(2):126-30
10194649
Proc Natl Acad Sci U S A. 1979 Nov;76(11):5962-6
293695
J Physiol. 2001 Dec 15;537(Pt 3):853-69
11744760
Proc Natl Acad Sci U S A. 2006 Dec 12;103(50):19188-93
17138670
J Neurophysiol. 2004 Jan;91(1):267-73
14715720
Neuron. 2000 Jan;25(1):123-8
10707977
Neuron. 1995 Apr;14(4):697-706
7718233
J Physiol. 2002 Jan 1;538(Pt 1):227-51
11773331
Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Sep;68(3 Pt 1):031907
14524803
Nature. 2002 Mar 21;416(6878):286-90
11875398
Cell. 2007 May 4;129(3):605-16
17482552
J Neurosci. 1999 Mar 15;19(6):2152-60
10066268
Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Jul;70(1 Pt 1):011908
15324089
J Neurophysiol. 2002 Feb;87(2):834-44
11826050
Neurosci Lett. 1993 Jul 23;157(2):199-202
8233053
Neuroscience. 2003;120(1):65-73
12849741
J Neurophysiol. 1997 Oct;78(4):2217-20
9325388
Brain Res. 1995 Jul 31;687(1-2):125-32
7583297
Nat Neurosci. 1998 Dec;1(8):708-13
10196587
J Physiol. 1998 Feb 1;506 ( Pt 3):775-93
9503337
Brain Res. 2000 Jun 2;866(1-2):247-56
10825500
Science. 1986 Nov 7;234(4777):738-40
3775364
Brain Res. 1972 Jul 13;42(1):201-6
5047187
J Neurosci. 2003 Jun 15;23(12):4831-41
12832505
Eur J Neurosci. 2004 May;19(10):2791-8
15147312
J Neurosci. 2003 Mar 1;23(5):1593-604
12629163
J Neurosci. 2004 Sep 15;24(37):7985-98
15371499
J Neurosci. 2006 Apr 19;26(16):4247-55
16624945
Nature. 1997 Jun 5;387(6633):598-603
9177347
J Neurophysiol. 2004 Jul;92(1):311-9
14973316
Brain Res Bull. 1990 Jul;25(1):93-8
2207720
Neuroscience. 1984 Nov;13(3):761-7
6098858
J Neurosci. 1999 Aug 1;19(15):6700-11
10414999
Neuroscience. 1995 Feb;64(3):813-9
7715789
Curr Biol. 2005 May 24;15(10):886-93
15916945
J Neurophysiol. 2003 Sep;90(3):1438-48
12750413
J Neurophysiol. 2003 Sep;90(3):1589-97
12966176
Pflugers Arch. 2006 Apr;452(1):7-15
16283205