 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, February 1, 2002, 22(3):1002-1009
Electrical Synapses in the Thalamic Reticular Nucleus
Carole E. Landisman1, Michael A. Long1, Michael Beierlein1, Michael R. Deans2, David L. Paul2, and Barry W. Connors1 1 Department of Neuroscience, Division of Biology and Medicine, Brown University, Providence, Rhode Island 02912, and 2 Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115
Neurons of the thalamic reticular nucleus (TRN) provide inhibitory input to thalamic relay cells and generate synchronized activity during sleep and seizures. It is widely assumed that TRN cells interact only via chemical synaptic connections. However, we show that many neighboring pairs of TRN neurons in rats and mice are electrically coupled. In paired-cell recordings, electrical synapses were able to mediate close correlations between action potentials when the coupling was strong; they could modulate burst-firing states even when the coupling strength was more modest. Electrical synapses between TRN neurons were absent in mice with a null mutation for the connexin36 (Cx36) gene. Surprisingly, inhibitory chemical synaptic connections between pairs of neurons were not observed, although strong extracellular stimuli could evoke inhibition in single TRN neurons. We conclude that Cx36-dependent gap junctions play an important role in the regulation of neural firing patterns within the TRN. When combined with recent observations from the cerebral cortex, our results imply that electrical synapses are a common mechanism for generating synchrony within networks of inhibitory neurons in the mammalian forebrain.
Key words: thalamus; reticular nucleus; gap junctions; electrical coupling; connexin36; rat; mouse; inhibition; synchrony
Copyright © 2002 Society for Neuroscience 0270-6474/02/2231002-08$05.00/0
This article has been cited by other articles:
B. J. Maher, M. J. McGinley, and G. L. Westbrook
Experience-dependent maturation of the glomerular microcircuit
PNAS, September 29, 2009; 106(39): 16865 - 16870.
[Abstract] [Full Text] [PDF]
H.-W. Dong, A. Hayar, J. Callaway, X.-H. Yang, Q. Nai, and M. Ennis
Group I mGluR Activation Enhances Ca2+-Dependent Nonselective Cation Currents and Rhythmic Bursting in Main Olfactory Bulb External Tufted Cells
J. Neurosci., September 23, 2009; 29(38): 11943 - 11953.
[Abstract] [Full Text] [PDF]
P. R. L. Parker, S. J. Cruikshank, and B. W. Connors
Stability of Electrical Coupling despite Massive Developmental Changes of Intrinsic Neuronal Physiology
J. Neurosci., August 5, 2009; 29(31): 9761 - 9770.
[Abstract] [Full Text] [PDF]
K. R. Tovar, B. J. Maher, and G. L. Westbrook
Direct Actions of Carbenoxolone on Synaptic Transmission and Neuronal Membrane Properties
J Neurophysiol, August 1, 2009; 102(2): 974 - 978.
[Abstract] [Full Text] [PDF]
Y.-W. Lam and S. M. Sherman
Functional Organization of the Somatosensory Cortical Layer 6 Feedback to the Thalamus
Cereb Cortex, May 15, 2009; (2009) bhp077v1.
[Abstract] [Full Text] [PDF]
W.-C. Li, A. Roberts, and S. R. Soffe
Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles
J. Physiol., April 15, 2009; 587(8): 1677 - 1693.
[Abstract] [Full Text] [PDF]
T. Fukuda
Network Architecture of Gap Junction-Coupled Neuronal Linkage in the Striatum
J. Neurosci., January 28, 2009; 29(4): 1235 - 1243.
[Abstract] [Full Text] [PDF]
I. L. Hanganu, A. Okabe, V. Lessmann, and H. J. Luhmann
Cellular Mechanisms of Subplate-Driven and Cholinergic Input-Dependent Network Activity in the Neonatal Rat Somatosensory Cortex
Cereb Cortex, January 1, 2009; 19(1): 89 - 105.
[Abstract] [Full Text] [PDF]
D. Gonzalez-Nieto, J. M. Gomez-Hernandez, B. Larrosa, C. Gutierrez, M. D. Munoz, I. Fasciani, J. O'Brien, A. Zappala, F. Cicirata, and L. C. Barrio
Regulation of neuronal connexin-36 channels by pH
PNAS, November 4, 2008; 105(44): 17169 - 17174.
[Abstract] [Full Text] [PDF]
C. E. Landisman and B. W. Connors
VPM and PoM Nuclei of the Rat Somatosensory Thalamus: Intrinsic Neuronal Properties and Corticothalamic Feedback
Cereb Cortex, December 1, 2007; 17(12): 2853 - 2865.
[Abstract] [Full Text] [PDF]
M. Xu, C. H. Liu, Y. Xiong, and J. He
Corticofugal modulation of the auditory thalamic reticular nucleus of the guinea pig
J. Physiol., November 15, 2007; 585(1): 15 - 28.
[Abstract] [Full Text] [PDF]
Y.-W. Lam and S. M. Sherman
Different Topography of the Reticulothalmic Inputs to First- and Higher-Order Somatosensory Thalamic Relays Revealed Using Photostimulation
J Neurophysiol, November 1, 2007; 98(5): 2903 - 2909.
[Abstract] [Full Text] [PDF]
H. Barbas and B. Zikopoulos
The Prefrontal Cortex and Flexible Behavior
Neuroscientist, October 1, 2007; 13(5): 532 - 545.
[Abstract] [PDF]
D. S. Heister, A. Hayar, A. Charlesworth, C. Yates, Y.-H. Zhou, and E. Garcia-Rill
Evidence for Electrical Coupling in the SubCoeruleus (SubC) Nucleus
J Neurophysiol, April 1, 2007; 97(4): 3142 - 3147.
[Abstract] [Full Text] [PDF]
M. Ennis and S. Datta
Electrotonic Coupling in the Nucleus SubCoeruleus. Focus on "Evidence for Electrical Coupling in the SubCoeruleus (SubC) Nucleus"
J Neurophysiol, April 1, 2007; 97(4): 2579 - 2579.
[Full Text] [PDF]
Y.-W. Lam, C. S. Nelson, and S. M. Sherman
Mapping of the Functional Interconnections Between Thalamic Reticular Neurons Using Photostimulation
J Neurophysiol, November 1, 2006; 96(5): 2593 - 2600.
[Abstract] [Full Text] [PDF]
C. Deleuze and J. R. Huguenard
Distinct Electrical and Chemical Connectivity Maps in the Thalamic Reticular Nucleus: Potential Roles in Synchronization and Sensation.
J. Neurosci., August 15, 2006; 26(33): 8633 - 8645.
[Abstract] [Full Text] [PDF]
B. Zikopoulos and H. Barbas
Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms.
J. Neurosci., July 12, 2006; 26(28): 7348 - 7361.
[Abstract] [Full Text] [PDF]
H. Khosravani and G. W. Zamponi
Voltage-gated calcium channels and idiopathic generalized epilepsies.
Physiol Rev, July 1, 2006; 86(3): 941 - 966.
[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]
K. L. Blethyn, S. W. Hughes, T. I. Toth, D. W. Cope, and V. Crunelli
Neuronal Basis of the Slow (<1 Hz) Oscillation in Neurons of the Nucleus Reticularis Thalami In Vitro
J. Neurosci., March 1, 2006; 26(9): 2474 - 2486.
[Abstract] [Full Text] [PDF]
V. S. Sohal and J. R. Huguenard
Inhibitory coupling specifically generates emergent gamma oscillations in diverse cell types
PNAS, December 20, 2005; 102(51): 18638 - 18643.
[Abstract] [Full Text] [PDF]
C. E. Landisman and B. W. Connors
Long-Term Modulation of Electrical Synapses in the Mammalian Thalamus
Science, December 16, 2005; 310(5755): 1809 - 1813.
[Abstract] [Full Text] [PDF]
Y.-W. Lam and S. M. Sherman
Mapping by Laser Photostimulation of Connections Between the Thalamic Reticular and Ventral Posterior Lateral Nuclei in the Rat
J Neurophysiol, October 1, 2005; 94(4): 2472 - 2483.
[Abstract] [Full Text] [PDF]
C. Soto-Trevino, P. Rabbah, E. Marder, and F. Nadim
Computational Model of Electrically Coupled, Intrinsically Distinct Pacemaker Neurons
J Neurophysiol, July 1, 2005; 94(1): 590 - 604.
[Abstract] [Full Text] [PDF]
F. C Crick and C. Koch
What is the function of the claustrum?
Phil Trans R Soc B, June 29, 2005; 360(1458): 1271 - 1279.
[Abstract] [Full Text] [PDF]
J. Zhang and S. M. Wu
Physiological properties of rod photoreceptor electrical coupling in the tiger salamander retina
J. Physiol., May 1, 2005; 564(3): 849 - 862.
[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]
E. Sharifullina, K. Ostroumov, and A. Nistri
Metabotropic glutamate receptor activity induces a novel oscillatory pattern in neonatal rat hypoglossal motoneurones
J. Physiol., February 15, 2005; 563(1): 139 - 159.
[Abstract] [Full Text] [PDF]
M. Vandecasteele, J. Glowinski, and L. Venance
Electrical Synapses between Dopaminergic Neurons of the Substantia Nigra Pars Compacta
J. Neurosci., January 12, 2005; 25(2): 291 - 298.
[Abstract] [Full Text] [PDF]
N. Kopell and B. Ermentrout
Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks
PNAS, October 26, 2004; 101(43): 15482 - 15487.
[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]
S. J. Cruikshank, M. Hopperstad, M. Younger, B. W. Connors, D. C. Spray, and M. Srinivas
Potent block of Cx36 and Cx50 gap junction channels by mefloquine
PNAS, August 17, 2004; 101(33): 12364 - 12369.
[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]
E. Masaki, M. Kawamura, and F. Kato
Attenuation of Gap-Junction-Mediated Signaling Facilitated Anesthetic Effect of Sevoflurane in the Central Nervous System of Rats
Anesth. Analg., March 1, 2004; 98(3): 647 - 652.
[Abstract] [Full Text] [PDF]
L. Zhang and E. G. Jones
Corticothalamic Inhibition in the Thalamic Reticular Nucleus
J Neurophysiol, February 1, 2004; 91(2): 759 - 766.
[Abstract] [Full Text] [PDF]
M. A. Long, C. E. Landisman, and B. W. Connors
Small Clusters of Electrically Coupled Neurons Generate Synchronous Rhythms in the Thalamic Reticular Nucleus
J. Neurosci., January 14, 2004; 24(2): 341 - 349.
[Abstract] [Full Text] [PDF]
R. Bruzzone, S. G. Hormuzdi, M. T. Barbe, A. Herb, and H. Monyer
Pannexins, a family of gap junction proteins expressed in brain
PNAS, November 11, 2003; 100(23): 13644 - 13649.
[Abstract] [Full Text] [PDF]
A. DESTEXHE and T. J. SEJNOWSKI
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations
Physiol Rev, October 1, 2003; 83(4): 1401 - 1453.
[Abstract] [Full Text] [PDF]
A. Pereda, J. O'Brien, J. I. Nagy, F. Bukauskas, K. G. V. Davidson, N. Kamasawa, T. Yasumura, and J. E. Rash
Connexin35 Mediates Electrical Transmission at Mixed Synapses on Mauthner Cells
J. Neurosci., August 20, 2003; 23(20): 7489 - 7503.
[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. A. Hartings, S. Temereanca, and D. J. Simons
State-Dependent Processing of Sensory Stimuli by Thalamic Reticular Neurons
J. Neurosci., June 15, 2003; 23(12): 5264 - 5271.
[Abstract] [Full Text] [PDF]
D. Friedman and B. W. Strowbridge
Both Electrical and Chemical Synapses Mediate Fast Network Oscillations in the Olfactory Bulb
J Neurophysiol, May 1, 2003; 89(5): 2601 - 2610.
[Abstract] [Full Text] [PDF]
L. J Gentet and D. Ulrich
Strong, reliable and precise synaptic connections between thalamic relay cells and neurones of the nucleus reticularis in juvenile rats
J. Physiol., February 1, 2003; 546(3): 801 - 811.
[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. A. Long, M. R. Deans, D. L. Paul, and B. W. Connors
Rhythmicity without Synchrony in the Electrically Uncoupled Inferior Olive
J. Neurosci., December 15, 2002; 22(24): 10898 - 10905.
[Abstract] [Full Text] [PDF]
A. H. Meyer, I. Katona, M. Blatow, A. Rozov, and H. Monyer
In Vivo Labeling of Parvalbumin-Positive Interneurons and Analysis of Electrical Coupling in Identified Neurons
J. Neurosci., August 15, 2002; 22(16): 7055 - 7064.
[Abstract] [Full Text] [PDF]
Y. Shu and D. A. McCormick
Inhibitory Interactions Between Ferret Thalamic Reticular Neurons
J Neurophysiol, May 1, 2002; 87(5): 2571 - 2576.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|