 |
Previous Article | Next Article 
The Journal of Neuroscience, May 1, 1999, 19(9):3298-3306
Electrotonic Coupling Interacts with Intrinsic Properties to
Generate Synchronized Activity in Cerebellar Networks of Inhibitory
Interneurons
Puah
Mann-Metzer and
Yosef
Yarom
Department of Neurobiology, Life Science Institute and Center for
Neural Computation, Hebrew University, Jerusalem 91904, Israel
Exploring the organization and function of local inhibitory
networks is an essential step on the way to understand the principles of brain operation. We show here that molecular layer inhibitory interneurons of the guinea pig cerebellar cortex are organized as local
networks, generating synchronous activity. Simultaneous recording from
two adjacent interneurons revealed a direct current flow between
synchronized pairs of neurons. Blocking inhibitory or excitatory
synaptic transmission did not alter the synchronization. The
electrotonic coupling coefficient (average 0.1) depended mainly on the
input resistance of the postsynaptic cell, indicating a homogenous
coupling resistance between different pairs. A presynaptic action
potential generated a short, attenuated spikelet in the postsynaptic
cell. The passive current flow was amplified by voltage-dependent intrinsic currents to create a reciprocal interplay between the presynaptic and postsynaptic cells. This interplay results in a time
window for synchronization that is wider than expected from the
duration of the spikelet. Intracellular staining with biocytin revealed
high incidence of dye coupling. Furthermore, the interneurons located
superficially in the molecular layer tend to form larger networks
compared with the inner interneurons. We propose that weakly coupled
inhibitory networks can generate loosely synchronous activity, which
results from the interaction of electrical coupling and intrinsic currents.
Key words:
cerebellum; electrotonic coupling; synchronization; inhibitory network; inhibitory interneurons; dye coupling
Copyright © 1999 Society for Neuroscience 0270-6474/99/1993298-09$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
P. M. Lachamp, Y. Liu, and S. J. Liu
Glutamatergic Modulation of Cerebellar Interneuron Activity Is Mediated by an Enhancement of GABA Release and Requires Protein Kinase A/RIM1{alpha} Signaling
J. Neurosci.,
January 14, 2009;
29(2):
381 - 392.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Chen, L. S. Popa, X. Wang, W. Gao, J. Barnes, C. M. Hendrix, E. J. Hess, and T. J. Ebner
Low-Frequency Oscillations in the Cerebellar Cortex of the Tottering Mouse
J Neurophysiol,
January 1, 2009;
101(1):
234 - 245.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Veruki, L. Oltedal, and E. Hartveit
Electrical Synapses Between AII Amacrine Cells: Dynamic Range and Functional Consequences of Variation in Junctional Conductance
J Neurophysiol,
December 1, 2008;
100(6):
3305 - 3322.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Gelenbe and S. Timotheou
Synchronized Interactions in Spiked Neuronal Networks
The Computer Journal,
November 1, 2008;
51(6):
723 - 730.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S.-H. Tseng, L.-Y. Tsai, and S.-R. Yeh
Induction of High-Frequency Oscillations in a Junction-Coupled Network
J. Neurosci.,
July 9, 2008;
28(28):
7165 - 7173.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Haneda and Y. Oka
Coordinated Synchronization in the Electrically Coupled Network of Terminal Nerve Gonadotropin-Releasing Hormone Neurons as Demonstrated by Double Patch-Clamp Study
Endocrinology,
July 1, 2008;
149(7):
3540 - 3548.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Rela and L. Szczupak
In Situ Characterization of a Rectifying Electrical Junction
J Neurophysiol,
February 1, 2007;
97(2):
1405 - 1412.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Hinckley and L. Ziskind-Conhaim
Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord.
J. Neurosci.,
August 15, 2006;
26(33):
8477 - 8483.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. I. Aller, E. L. Veale, A.-M. Linden, C. Sandu, M. Schwaninger, L. J. Evans, E. R. Korpi, A. Mathie, W. Wisden, and S. G. Brickley
Modifying the Subunit Composition of TASK Channels Alters the Modulation of a Leak Conductance in Cerebellar Granule Neurons
J. Neurosci.,
December 7, 2005;
25(49):
11455 - 11467.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Hayar, M. T. Shipley, and M. Ennis
Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms
J. Neurosci.,
September 7, 2005;
25(36):
8197 - 8208.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Price, B. Cauli, E. R. Kovacs, A. Kulik, B. Lambolez, R. Shigemoto, and M. Capogna
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
J. Neurosci.,
July 20, 2005;
25(29):
6775 - 6786.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. P. Dugue, A. Dumoulin, A. Triller, and S. Dieudonne
Target-Dependent Use of Coreleased Inhibitory Transmitters at Central Synapses
J. Neurosci.,
July 13, 2005;
25(28):
6490 - 6498.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Hidaka, Y. Akahori, and Y. Kurosawa
Dendrodendritic Electrical Synapses between Mammalian Retinal Ganglion Cells
J. Neurosci.,
November 17, 2004;
24(46):
10553 - 10567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Crochet, P. Fuentealba, I. Timofeev, and M. Steriade
Selective Amplification of Neocortical Neuronal Output by Fast Prepotentials InVivo
Cereb Cortex,
October 1, 2004;
14(10):
1110 - 1121.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-L. Zhang, L. Zhang, and P. L. Carlen
Electrotonic coupling between stratum oriens interneurones in the intact in vitro mouse juvenile hippocampus
J. Physiol.,
August 1, 2004;
558(3):
825 - 839.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Hayar, S. Karnup, M. Ennis, and M. T. Shipley
External Tufted Cells: A Major Excitatory Element That Coordinates Glomerular Activity
J. Neurosci.,
July 28, 2004;
24(30):
6676 - 6685.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Curti and A. E. Pereda
Voltage-Dependent Enhancement of Electrical Coupling by a Subthreshold Sodium Current
J. Neurosci.,
April 21, 2004;
24(16):
3999 - 4010.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Feigenspan, U. Janssen-Bienhold, S. Hormuzdi, H. Monyer, J. Degen, G. Sohl, K. Willecke, J. Ammermuller, and R. Weiler
Expression of Connexin36 in Cone Pedicles and OFF-Cone Bipolar Cells of the Mouse Retina
J. Neurosci.,
March 31, 2004;
24(13):
3325 - 3334.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cheron, D. Gall, L. Servais, B. Dan, R. Maex, and S. N. Schiffmann
Inactivation of Calcium-Binding Protein Genes Induces 160 Hz Oscillations in the Cerebellar Cortex of Alert Mice
J. Neurosci.,
January 14, 2004;
24(2):
434 - 441.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Mamiya, Y. Manor, and F. Nadim
Short-Term Dynamics of a Mixed Chemical and Electrical Synapse in a Rhythmic Network
J. Neurosci.,
October 22, 2003;
23(29):
9557 - 9564.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Jorntell and C.-F. Ekerot
Receptive Field Plasticity Profoundly Alters the Cutaneous Parallel Fiber Synaptic Input to Cerebellar Interneurons In Vivo
J. Neurosci.,
October 22, 2003;
23(29):
9620 - 9631.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Gauck and D. Jaeger
The Contribution of NMDA and AMPA Conductances to the Control of Spiking in Neurons of the Deep Cerebellar Nuclei
J. Neurosci.,
September 3, 2003;
23(22):
8109 - 8118.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Pfeuty, G. Mato, D. Golomb, and D. Hansel
Electrical Synapses and Synchrony: The Role of Intrinsic Currents
J. Neurosci.,
July 16, 2003;
23(15):
6280 - 6294.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Chavas and A. Marty
Coexistence of Excitatory and Inhibitory GABA Synapses in the Cerebellar Interneuron Network
J. Neurosci.,
March 15, 2003;
23(6):
2019 - 2031.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Rela and L. Szczupak
Coactivation of Motoneurons Regulated by a Network Combining Electrical and Chemical Synapses
J. Neurosci.,
January 15, 2003;
23(2):
682 - 692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Tresch and O. Kiehn
Synchronization of Motor Neurons during Locomotion in the Neonatal Rat: Predictors and Mechanisms
J. Neurosci.,
November 15, 2002;
22(22):
9997 - 10008.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. S. Jahromi, K. Wentlandt, S. Piran, and P. L. Carlen
Anticonvulsant Actions of Gap Junctional Blockers in an In Vitro Seizure Model
J Neurophysiol,
October 1, 2002;
88(4):
1893 - 1902.
[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]
|
 |
|

|
 |

|
 |
 
B. A. Clark and S. G. Cull-Candy
Activity-Dependent Recruitment of Extrasynaptic NMDA Receptor Activation at an AMPA Receptor-Only Synapse
J. Neurosci.,
June 1, 2002;
22(11):
4428 - 4436.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Mann-Metzer and Y. Yarom
Jittery Trains Induced by Synaptic-Like Currents in Cerebellar Inhibitory Interneurons
J Neurophysiol,
January 1, 2002;
87(1):
149 - 156.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Mann-Metzer and Y. Yarom
Pre- and Postsynaptic Inhibition Mediated by GABAB Receptors in Cerebellar Inhibitory Interneurons
J Neurophysiol,
January 1, 2002;
87(1):
183 - 190.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Nusser, L. M. Kay, G. Laurent, G. E. Homanics, and I. Mody
Disruption of GABAA Receptors on GABAergic Interneurons Leads to Increased Oscillatory Power in the Olfactory Bulb Network
J Neurophysiol,
December 1, 2001;
86(6):
2823 - 2833.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Arisi, D. Zoccolan, and V. Torre
Distributed Motor Pattern Underlying Whole-Body Shortening in the Medicinal Leech
J Neurophysiol,
November 1, 2001;
86(5):
2475 - 2488.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. H. Singer, R. R. Mirotznik, and M. B. Feller
Potentiation of L-Type Calcium Channels Reveals Nonsynaptic Mechanisms that Correlate Spontaneous Activity in the Developing Mammalian Retina
J. Neurosci.,
November 1, 2001;
21(21):
8514 - 8522.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Guldenagel, J. Ammermuller, A. Feigenspan, B. Teubner, J. Degen, G. Sohl, K. Willecke, and R. Weiler
Visual Transmission Deficits in Mice with Targeted Disruption of the Gap Junction Gene Connexin36
J. Neurosci.,
August 15, 2001;
21(16):
6036 - 6044.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Szabadics, A. Lorincz, and G. Tamas
{beta}and {gamma} Frequency Synchronization by Dendritic GABAergic Synapses and Gap Junctions in a Network of Cortical Interneurons
J. Neurosci.,
August 1, 2001;
21(15):
5824 - 5831.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Loewenstein, Y. Yarom, and H. Sompolinsky
The generation of oscillations in networks of electrically coupled cells
PNAS,
June 20, 2001;
(2001)
131116898.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Ermentrout, J. W. Wang, J. Flores, and A. Gelperin
Model for Olfactory Discrimination and Learning in Limax Procerebrum Incorporating Oscillatory Dynamics and Wave Propagation
J Neurophysiol,
April 1, 2001;
85(4):
1444 - 1452.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Traub, R. Bibbig, A. Piechotta, R. Draguhn, and D. Schmitz
Synaptic and Nonsynaptic Contributions to Giant IPSPs and Ectopic Spikes Induced by 4-Aminopyridine in the Hippocampus In Vitro
J Neurophysiol,
March 1, 2001;
85(3):
1246 - 1256.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. F. De-Miguel, M. Vargas-Caballero, and E. Garcia-Perez
Spread of synaptic potentials through electrical synapses in Retzius neurones of the leech
J. Exp. Biol.,
January 10, 2001;
204(19):
3241 - 3250.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. T. Dickson, G. Biella, and M. de Curtis
Evidence for Spatial Modules Mediated by Temporal Synchronization of Carbachol-Induced Gamma Rhythm in Medial Entorhinal Cortex
J. Neurosci.,
October 15, 2000;
20(20):
7846 - 7854.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Venance, A. Rozov, M. Blatow, N. Burnashev, D. Feldmeyer, and H. Monyer
Connexin expression in electrically coupled postnatal rat brain neurons
PNAS,
August 10, 2000;
(2000)
160037097.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. Cohen and Y. Yarom
Cerebellar On-Beam and Lateral Inhibition: Two Functionally Distinct Circuits
J Neurophysiol,
April 1, 2000;
83(4):
1932 - 1940.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q. Chang, A. Pereda, M. J. Pinter, and R. J. Balice-Gordon
Nerve Injury Induces Gap Junctional Coupling among Axotomized Adult Motor Neurons
J. Neurosci.,
January 15, 2000;
20(2):
674 - 684.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. Pedroarena, I. E. Pose, J. Yamuy, M. H. Chase, and F. R. Morales
Oscillatory Membrane Potential Activity in the Soma of a Primary Afferent Neuron
J Neurophysiol,
September 1, 1999;
82(3):
1465 - 1476.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Loewenstein, Y. Yarom, and H. Sompolinsky
The generation of oscillations in networks of electrically coupled cells
PNAS,
July 3, 2001;
98(14):
8095 - 8100.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Venance, A. Rozov, M. Blatow, N. Burnashev, D. Feldmeyer, and H. Monyer
Connexin expression in electrically coupled postnatal rat brain neurons
PNAS,
August 29, 2000;
97(18):
10260 - 10265.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|