 |
Previous Article | Next Article 
The Journal of Neuroscience, April 15, 2001, 21(8):2687-2698
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus
Interneuron Network
Marlene
Bartos1,
Imre
Vida2,
Michael
Frotscher2,
Jörg R. P.
Geiger1, and
Peter
Jonas1
1 Physiologisches Institut and
2 Anatomisches Institut, Albert-Ludwigs-Universität
Freiburg, D-79104 Freiburg, Germany
Mutual synaptic interactions between GABAergic interneurons are
thought to be of critical importance for the generation of network
oscillations and for temporal encoding of information in the
hippocampus. However, the functional properties of synaptic transmission between hippocampal interneurons are largely unknown. We
have made paired recordings from basket cells (BCs) in the dentate
gyrus of rat hippocampal slices, followed by correlated light and
electron microscopical analysis. Unitary GABAA
receptor-mediated IPSCs at BC-BC synapses recorded at the soma showed
a fast rise and decay, with a mean decay time constant of 2.5 ± 0.2 msec (32°C). Synaptic transmission at BC-BC synapses showed
paired-pulse depression (PPD) (32 ± 5% for 10 msec interpulse
intervals) and multiple-pulse depression during repetitive stimulation.
Detailed passive cable model simulations based on somatodendritic
morphology and localization of synaptic contacts further indicated that
the conductance change at the postsynaptic site was even faster,
decaying with a mean time constant of 1.8 ± 0.6 msec. Sequential
triple recordings revealed that the decay time course of IPSCs at
BC-BC synapses was approximately twofold faster than that at
BC-granule cell synapses, whereas the extent of PPD was comparable. To
examine the consequences of the fast postsynaptic conductance change
for the generation of oscillatory activity, we developed a
computational model of an interneuron network. The model showed robust
oscillations at frequencies >60 Hz if the excitatory drive was
sufficiently large. Thus the fast conductance change at
interneuron-interneuron synapses may promote the generation of
high-frequency oscillations observed in the dentate gyrus
in vivo.
Key words:
GABAergic interneurons; basket cells; dentate gyrus; unitary IPSCs; paired-pulse depression; paired recording; interneuron
networks; gamma oscillations; computational model
Copyright © 2001 Society for Neuroscience 0270-6474/01/2182687-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
P. Li, U. Rudolph, and M. M. Huntsman
Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex
PNAS,
July 21, 2009;
106(29):
12156 - 12161.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Zhang and P. S. Buckmaster
Dysfunction of the Dentate Basket Cell Circuit in a Rat Model of Temporal Lobe Epilepsy
J. Neurosci.,
June 17, 2009;
29(24):
7846 - 7856.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Achuthan and C. C. Canavier
Phase-Resetting Curves Determine Synchronization, Phase Locking, and Clustering in Networks of Neural Oscillators
J. Neurosci.,
April 22, 2009;
29(16):
5218 - 5233.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Doischer, J. Aurel Hosp, Y. Yanagawa, K. Obata, P. Jonas, I. Vida, and M. Bartos
Postnatal Differentiation of Basket Cells from Slow to Fast Signaling Devices
J. Neurosci.,
November 26, 2008;
28(48):
12956 - 12968.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Galarreta, F. Erdelyi, G. Szabo, and S. Hestrin
Cannabinoid Sensitivity and Synaptic Properties of 2 GABAergic Networks in the Neocortex
Cereb Cortex,
October 1, 2008;
18(10):
2296 - 2305.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. J. Urbano, E. Leznik, and R. R. Llinas
Modafinil enhances thalamocortical activity by increasing neuronal electrotonic coupling
PNAS,
July 24, 2007;
104(30):
12554 - 12559.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Dyhrfjeld-Johnsen, V. Santhakumar, R. J. Morgan, R. Huerta, L. Tsimring, and I. Soltesz
Topological Determinants of Epileptogenesis in Large-Scale Structural and Functional Models of the Dentate Gyrus Derived From Experimental Data
J Neurophysiol,
February 1, 2007;
97(2):
1566 - 1587.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Woodruff and P. Sah
Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala
J. Neurosci.,
January 17, 2007;
27(3):
553 - 563.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Kerr and M. Capogna
Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus
J. Physiol.,
January 15, 2007;
578(2):
451 - 470.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Zsiros, I. Aradi, and G. Maccaferri
Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus
J. Physiol.,
January 15, 2007;
578(2):
527 - 544.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Halabisky, F. Shen, J. R. Huguenard, and D. A. Prince
Electrophysiological Classification of Somatostatin-Positive Interneurons in Mouse Sensorimotor Cortex
J Neurophysiol,
August 1, 2006;
96(2):
834 - 845.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. M. Huntsman and J. R. Huguenard
Fast IPSCs in rat thalamic reticular nucleus require the GABAA receptor {beta}1 subunit
J. Physiol.,
April 15, 2006;
572(2):
459 - 475.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. F. Safiulina, G. Fattorini, F. Conti, and E. Cherubini
GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus
J. Neurosci.,
January 11, 2006;
26(2):
597 - 608.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Geisler, N. Brunel, and X.-J. Wang
Contributions of Intrinsic Membrane Dynamics to Fast Network Oscillations With Irregular Neuronal Discharges
J Neurophysiol,
December 1, 2005;
94(6):
4344 - 4361.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Zsiros and G. Maccaferri
Electrical Coupling between Interneurons with Different Excitable Properties in the Stratum Lacunosum-Moleculare of the Juvenile CA1 Rat Hippocampus
J. Neurosci.,
September 21, 2005;
25(38):
8686 - 8695.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. K. Skinner, J.Y.J. Chung, I. Ncube, P. A. Murray, and S. A. Campbell
Using Heterogeneity to Predict Inhibitory Network Model Characteristics
J Neurophysiol,
April 1, 2005;
93(4):
1898 - 1907.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Traub, D. Contreras, M. O. Cunningham, H. Murray, F. E. N. LeBeau, A. Roopun, A. Bibbig, W. B. Wilent, M. J. Higley, and M. A. Whittington
Single-Column Thalamocortical Network Model Exhibiting Gamma Oscillations, Sleep Spindles, and Epileptogenic Bursts
J Neurophysiol,
April 1, 2005;
93(4):
2194 - 2232.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. L Garner, M. A Whittington, and Z. Henderson
Induction by kainate of theta frequency rhythmic activity in the rat medial septum-diagonal band complex in vitro
J. Physiol.,
April 1, 2005;
564(1):
83 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Santhakumar, I. Aradi, and I. Soltesz
Role of Mossy Fiber Sprouting and Mossy Cell Loss in Hyperexcitability: A Network Model of the Dentate Gyrus Incorporating Cell Types and Axonal Topography
J Neurophysiol,
January 1, 2005;
93(1):
437 - 453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Venance, J. Glowinski, and C. Giaume
Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices
J. Physiol.,
August 15, 2004;
559(1):
215 - 230.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Aradi, V. Santhakumar, and I. Soltesz
Impact of Heterogeneous Perisomatic IPSC Populations on Pyramidal Cell Firing Rates
J Neurophysiol,
June 1, 2004;
91(6):
2849 - 2858.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N Rouach, M Segal, A Koulakoff, C Giaume, and E Avignone
Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions
J. Physiol.,
December 15, 2003;
553(3):
729 - 745.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kulik, I. Vida, R. Lujan, C. A. Haas, G. Lopez-Bendito, R. Shigemoto, and M. Frotscher
Subcellular Localization of Metabotropic GABAB Receptor Subunits GABAB1a/b and GABAB2 in the Rat Hippocampus
J. Neurosci.,
December 3, 2003;
23(35):
11026 - 11035.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Maex and E. De Schutter
Resonant Synchronization in Heterogeneous Networks of Inhibitory Neurons
J. Neurosci.,
November 19, 2003;
23(33):
10503 - 10514.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Bacci, U. Rudolph, J. R. Huguenard, and D. A. Prince
Major Differences in Inhibitory Synaptic Transmission onto Two Neocortical Interneuron Subclasses
J. Neurosci.,
October 22, 2003;
23(29):
9664 - 9674.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Brunel and X.-J. Wang
What Determines the Frequency of Fast Network Oscillations With Irregular Neural Discharges? I. Synaptic Dynamics and Excitation-Inhibition Balance
J Neurophysiol,
July 1, 2003;
90(1):
415 - 430.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-C. Lien and P. Jonas
Kv3 Potassium Conductance is Necessary and Kinetically Optimized for High-Frequency Action Potential Generation in Hippocampal Interneurons
J. Neurosci.,
March 15, 2003;
23(6):
2058 - 2068.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. M. Baker, P. S. Pennefather, B. A. Orser, and F. K. Skinner
Disruption of Coherent Oscillations in Inhibitory Networks With Anesthetics: Role of GABAA Receptor Desensitization
J Neurophysiol,
November 1, 2002;
88(5):
2821 - 2833.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T Bianchi and R. L Macdonald
Slow phases of GABAA receptor desensitization: structural determinants and possible relevance for synaptic function
J. Physiol.,
October 1, 2002;
544(1):
3 - 18.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Bartos, I. Vida, M. Frotscher, A. Meyer, H. Monyer, J. R. P. Geiger, and P. Jonas
Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks
PNAS,
October 1, 2002;
99(20):
13222 - 13227.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Galarreta and S. Hestrin
Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex
PNAS,
September 17, 2002;
99(19):
12438 - 12443.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Klausberger, J. D. B. Roberts, and P. Somogyi
Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus
J. Neurosci.,
April 1, 2002;
22(7):
2513 - 2521.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Hefft, U. Kraushaar, J. R P Geiger, and P. Jonas
Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus
J. Physiol.,
February 15, 2002;
539(1):
201 - 208.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Traub, N. Kopell, A. Bibbig, E. H. Buhl, F. E. N. LeBeau, and M. A. Whittington
Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks
J. Neurosci.,
December 1, 2001;
21(23):
9478 - 9486.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|