 |
 Previous Article | Next Article 
The Journal of Neuroscience, January 1, 1998, 18(1):294-306
Blockade and Recovery of Spontaneous Rhythmic Activity after
Application of Neurotransmitter Antagonists to Spinal Networks of the
Chick Embryo
Nikolai
Chub and
Michael J.
O'Donovan
Section on Developmental Neurobiology, Laboratory of Neural
Control, National Institute of Neurological Diseases and Stroke,
National Institutes of Health, Bethesda, Maryland 20892
We studied the regulation of spontaneous activity in the embryonic
(day 10-11) chick spinal cord. After bath application of either an excitatory amino acid (AP-5 or CNQX) and a
nicotinic cholinergic (DH E or mecamylamine) antagonist,
or glycine and GABA receptor (bicuculline,
2-hydroxysaclofen, and strychnine) antagonists, spontaneous activity
was blocked for a period (30-90 min) but then reappeared in the
presence of the drugs. The efficacy of the antagonists was assessed by
their continued ability to block spinal reflex pathways during the
reappearance of spontaneous activity. Spontaneous activity ceased over
the 4-5 hour monitoring period when both sets of antagonists were
applied together.
After application of glycine and GABA receptor antagonists, the
frequency of occurrence of spontaneous episodes slowed and became
highly variable. By contrast, during glutamatergic and nicotinic
cholinergic blockade, the frequency of occurrence of spontaneous
episodes initially slowed and then recovered to stabilize near the
predrug level of activity. Whole-cell recordings made from ventral
spinal neurons revealed that this recovery was accompanied by an
increase in the amplitude of spontaneously occurring synaptic events.
We also measured changes in the apparent equilibrium potential of the
rhythmic, synaptic drive of ventral spinal neurons using voltage or
discontinuous current clamp. After excitatory blockade, the apparent
equilibrium potential of the rhythmic synaptic drive shifted ~10 mV
more negative to approximately  30 mV. In the presence of bicuculline,
the apparent equilibrium potential of the synaptic drive shifted toward
the glutamate equilibrium potential.
Considered with other evidence, these findings suggest that spontaneous
rhythmic output is a general property of developing spinal networks,
and that GABA and glycinergic networks alter their function to
compensate for the blockade of excitatory transmission.
Key words:
spinal plasticity; rhythmicity; embryonic networks; development; motoneurons; spontaneous neural activity
Copyright © 1998 Society for Neuroscience 0270-6474/98/181294-13$05.00/0
This article has been cited by other articles:
|
|
|
|
 
S. T. Sipila, K. Huttu, J. Yamada, R. Afzalov, J. Voipio, P. Blaesse, and K. Kaila
Compensatory Enhancement of Intrinsic Spiking upon NKCC1 Disruption in Neonatal Hippocampus
J. Neurosci.,
May 27, 2009;
29(21):
6982 - 6988.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Wilhelm, M. M. Rich, and P. Wenner
Compensatory changes in cellular excitability, not synaptic scaling, contribute to homeostatic recovery of embryonic network activity
PNAS,
April 21, 2009;
106(16):
6760 - 6765.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Gonzalez-Islas, N. Chub, and P. Wenner
NKCC1 and AE3 Appear to Accumulate Chloride in Embryonic Motoneurons
J Neurophysiol,
February 1, 2009;
101(2):
507 - 518.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Wilhelm and P. Wenner
GABAA transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude
PNAS,
August 12, 2008;
105(32):
11412 - 11417.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. S. Bradley, Y. U. Ryu, and J. Lin
Fast Locomotor Burst Generation in Late Stage Embryonic Motility
J Neurophysiol,
April 1, 2008;
99(4):
1733 - 1742.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Jean-Xavier, G. Z. Mentis, M. J. O'Donovan, D. Cattaert, and L. Vinay
Dual personality of GABA/glycine-mediated depolarizations in immature spinal cord
PNAS,
July 3, 2007;
104(27):
11477 - 11482.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Xu, A. Clement, T. M. Wright, and P. Wenner
Developmental Reorganization of the Output of a GABAergic Interneuronal Circuit
J Neurophysiol,
April 1, 2007;
97(4):
2769 - 2779.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. K. McCabe, S. L. Chisholm, H. L. Picken-Bahrey, and W. J. Moody
The self-regulating nature of spontaneous synchronized activity in developing mouse cortical neurones
J. Physiol.,
November 15, 2006;
577(1):
155 - 167.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. L. Pallas, P. Wenner, C. Gonzalez-Islas, M. Fagiolini, K. A. Razak, G. Kim, D. Sanes, and B. Roerig
Developmental Plasticity of Inhibitory Circuitry
J. Neurosci.,
October 11, 2006;
26(41):
10358 - 10361.
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Chub, G. Z. Mentis, and M. J. O'Donovan
Chloride-Sensitive MEQ Fluorescence in Chick Embryo Motoneurons Following Manipulations of Chloride and During Spontaneous Network Activity
J Neurophysiol,
January 1, 2006;
95(1):
323 - 330.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. C. Cowley, E. Zaporozhets, J. N. MacLean, and B. J. Schmidt
Is NMDA Receptor Activation Essential for the Production of Locomotor-Like Activity in the Neonatal Rat Spinal Cord?
J Neurophysiol,
December 1, 2005;
94(6):
3805 - 3814.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. S. Bradley, D. Solanki, and D. Zhao
Limb Movements During Embryonic Development in the Chick: Evidence for a Continuum in Limb Motor Control Antecedent to Locomotion
J Neurophysiol,
December 1, 2005;
94(6):
4401 - 4411.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. C. Stacy, J. Demas, R. W. Burgess, J. R. Sanes, and R. O. L. Wong
Disruption and Recovery of Patterned Retinal Activity in the Absence of Acetylcholine
J. Neurosci.,
October 12, 2005;
25(41):
9347 - 9357.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. N Hunt, A. K McCabe, and M. M Bosma
Midline serotonergic neurones contribute to widespread synchronized activity in embryonic mouse hindbrain
J. Physiol.,
August 1, 2005;
566(3):
807 - 819.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. J. Moody and M. M. Bosma
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells
Physiol Rev,
July 1, 2005;
85(3):
883 - 941.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Xu, P. J. Whelan, and P. Wenner
Development of an Inhibitory Interneuronal Circuit in the Embryonic Spinal Cord
J Neurophysiol,
May 1, 2005;
93(5):
2922 - 2933.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Thoby-Brisson, J.-B. Trinh, J. Champagnat, and G. Fortin
Emergence of the Pre-Botzinger Respiratory Rhythm Generator in the Mouse Embryo
J. Neurosci.,
April 27, 2005;
25(17):
4307 - 4318.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Marchetti, J. Tabak, N. Chub, M. J. O'Donovan, and J. Rinzel
Modeling Spontaneous Activity in the Developing Spinal Cord Using Activity-Dependent Variations of Intracellular Chloride
J. Neurosci.,
April 6, 2005;
25(14):
3601 - 3612.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Bonnot, G. Z. Mentis, J. Skoch, and M. J. O'Donovan
Electroporation Loading of Calcium-Sensitive Dyes Into the CNS
J Neurophysiol,
March 1, 2005;
93(3):
1793 - 1808.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. P. Calderon, N. Leverkova, and A. Peinado
Gq/11-Induced and Spontaneous Waves of Coordinated Network Activation in Developing Frontal Cortex
J. Neurosci.,
February 16, 2005;
25(7):
1737 - 1749.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Gonzalez-Forero, A. M. Pastor, E. J. Geiman, B. Benitez-Temino, and F. J. Alvarez
Regulation of Gephyrin Cluster Size and Inhibitory Synaptic Currents on Renshaw Cells by Motor Axon Excitatory Inputs
J. Neurosci.,
January 12, 2005;
25(2):
417 - 429.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. H. Casavant, C. M. Colbert, and S. E. Dryer
A-Current Expression is Regulated by Activity but not by Target Tissues in Developing Lumbar Motoneurons of the Chick Embryo
J Neurophysiol,
November 1, 2004;
92(5):
2644 - 2651.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. M. Syed, S. Lee, J. Zheng, and Z. J. Zhou
Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina
J. Physiol.,
October 15, 2004;
560(2):
533 - 549.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Luther, A. A. Robie, J. Yarotsky, C. Reina, E. Marder, and J. Golowasch
Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network
J Neurophysiol,
October 1, 2003;
90(4):
2720 - 2730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. G. Hanson and L. T. Landmesser
Characterization of the Circuits That Generate Spontaneous Episodes of Activity in the Early Embryonic Mouse Spinal Cord
J. Neurosci.,
January 15, 2003;
23(2):
587 - 600.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Momose-Sato, N. Miyakawa, H. Mochida, S. Sasaki, and K. Sato
Optical Analysis of Depolarization Waves in the Embryonic Brain: A Dual Network of Gap Junctions and Chemical Synapses
J Neurophysiol,
January 1, 2003;
89(1):
600 - 614.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Gabbay, I. Delvolve, and A. Lev-Tov
Pattern Generation in Caudal-Lumbar and Sacrococcygeal Segments of the Neonatal Rat Spinal Cord
J Neurophysiol,
August 1, 2002;
88(2):
732 - 739.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R J A Wilson, K Vasilakos, M B Harris, C Straus, and J E Remmers
Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators
J. Physiol.,
April 15, 2002;
540(2):
557 - 570.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Tabak, J. Rinzel, and M. J. O'Donovan
The Role of Activity-Dependent Network Depression in the Expression and Self-Regulation of Spontaneous Activity in the Developing Spinal Cord
J. Neurosci.,
November 15, 2001;
21(22):
8966 - 8978.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. S. Bradley
Age-Related Changes and Condition-Dependent Modifications in Distribution of Limb Movements During Embryonic Motility
J Neurophysiol,
October 1, 2001;
86(4):
1511 - 1522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Wenner and M. J. O'Donovan
Mechanisms That Initiate Spontaneous Network Activity in the Developing Chick Spinal Cord
J Neurophysiol,
September 1, 2001;
86(3):
1481 - 1498.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Chub and M. J. O'Donovan
Post-Episode Depression of GABAergic Transmission in Spinal Neurons of the Chick Embryo
J Neurophysiol,
May 1, 2001;
85(5):
2166 - 2176.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Bansal, J. H. Singer, B. J. Hwang, W. Xu, A. Beaudet, and M. B. Feller
Mice Lacking Specific Nicotinic Acetylcholine Receptor Subunits Exhibit Dramatically Altered Spontaneous Activity Patterns and Reveal a Limited Role for Retinal Waves in Forming ON and OFF Circuits in the Inner Retina
J. Neurosci.,
October 15, 2000;
20(20):
7672 - 7681.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. J. Zhou and D. Zhao
Coordinated Transitions in Neurotransmitter Systems for the Initiation and Propagation of Spontaneous Retinal Waves
J. Neurosci.,
September 1, 2000;
20(17):
6570 - 6577.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Saint-Amant and P. Drapeau
Motoneuron Activity Patterns Related to the Earliest Behavior of the Zebrafish Embryo
J. Neurosci.,
June 1, 2000;
20(11):
3964 - 3972.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Tabak, W. Senn, M. J. O'Donovan, and J. Rinzel
Modeling of Spontaneous Activity in Developing Spinal Cord Using Activity-Dependent Depression in an Excitatory Network
J. Neurosci.,
April 15, 2000;
20(8):
3041 - 3056.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Galante, A. Nistri, and L. Ballerini
Opposite changes in synaptic activity of organotypic rat spinal cord cultures after chronic block of AMPA/kainate or glycine and GABAA receptors
J. Physiol.,
March 15, 2000;
523(3):
639 - 651.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. T. Wong, K. L. Myhr, E. D. Miller, and R. O. L. Wong
Developmental Changes in the Neurotransmitter Regulation of Correlated Spontaneous Retinal Activity
J. Neurosci.,
January 1, 2000;
20(1):
351 - 360.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. E. Moore, N. Chub, J. Tabak, and M. O'Donovan
NMDA-Induced Dendritic Oscillations during a Soma Voltage Clamp of Chick Spinal Neurons
J. Neurosci.,
October 1, 1999;
19(19):
8271 - 8280.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. F. Usiak and L. T. Landmesser
Neuromuscular Activity Blockade Induced by Muscimol and d-Tubocurarine Differentially Affects the Survival of Embryonic Chick Motoneurons
J. Neurosci.,
September 15, 1999;
19(18):
7925 - 7939.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Wenner and M. J. O'Donovan
Identification of an Interneuronal Population that Mediates Recurrent Inhibition of Motoneurons in the Developing Chick Spinal Cord
J. Neurosci.,
September 1, 1999;
19(17):
7557 - 7567.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. d. l. Prida and J. V. Sanchez-Andres
Nonlinear Frequency-Dependent Synchronization in the Developing Hippocampus
J Neurophysiol,
July 1, 1999;
82(1):
202 - 208.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Ballerini, M. Galante, M. Grandolfo, and A. Nistri
Generation of rhythmic patterns of activity by ventral interneurones in rat organotypic spinal slice culture
J. Physiol.,
June 1, 1999;
517(2):
459 - 475.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. D. Milner and L. T. Landmesser
Cholinergic and GABAergic Inputs Drive Patterned Spontaneous Motoneuron Activity before Target Contact
J. Neurosci.,
April 15, 1999;
19(8):
3007 - 3022.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. S. Bradley
Transformations in Embryonic Motility in Chick: Kinematic Correlates of Type I and II Motility at E9 and E12
J Neurophysiol,
April 1, 1999;
81(4):
1486 - 1494.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Fedirchuk, P. Wenner, P. J. Whelan, S. Ho, J. Tabak, and M. J. O'Donovan
Spontaneous Network Activity Transiently Depresses Synaptic Transmission in the Embryonic Chick Spinal Cord
J. Neurosci.,
March 15, 1999;
19(6):
2102 - 2112.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. O'Donovan
Review : Robustness and Self-regulation in the Production of Neural Activity by Developing Networks
Neuroscientist,
January 1, 1999;
5(1):
41 - 47.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R J A Wilson, K Vasilakos, M B Harris, C Straus, and J E Remmers
Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators
J. Physiol.,
April 15, 2002;
540(2):
557 - 570.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
