Abstract
1. The well-developed cytoarchitecture of rat organotypic spinal cord culture makes it a suitable model to explore how persistent suppression of certain synaptic inputs might be compensated by increased synaptic efficacy (homeostatic plasticity). 2. Spontaneous or electrically evoked synaptic transmission of patch-clamped ventral horn interneurons was studied in control solution after blocking, for the second week in culture, AMPA/kainate receptors with CNQX or glycine and GABAA receptors with strychnine and bicuculline, or indiscriminately removing inputs with tetrodotoxin (TTX). 3. In untreated cells, spontaneous postsynaptic currents (PSCs) had fast (tau < 5 ms) or slow (tau > 10 ms) decay. A similar separation was observed when recording miniature currents (mPSCs). Slow decay PSCs were suppressed by strychnine plus bicuculline while fast decay events were eliminated by CNQX. 4. After chronic CNQX treatment the frequency of spontaneous, fast PSCs (of larger amplitude) or mPSCs was almost doubled with respect to control. These events were blocked by acutely applied CNQX, which unmasked slow PSCs. 5. After chronic TTX treatment neither the frequency nor the amplitude of spontaneous events was changed. 6. After chronic strychnine and bicuculline treatment the frequency and amplitude of all PSCs was decreased in most cells. mPSCs were also decreased in frequency. Spontaneous or electrically evoked currents acquired a larger component mediated by NMDA receptor activity. 7. The developing spinal network thus operated distinct homeostatic processes which led to strong enhancement in glutamatergic transmission after CNQX block or to broad downregulation of synaptic activity following chronic exposure to strychnine and bicuculline.
MeSH Terms
6-Cyano-7-nitroquinoxaline-2,3-dione/pharmacology
Animals
Bicuculline/pharmacology
Drug Combinations
Electric Conductivity
Excitatory Amino Acid Antagonists/pharmacology
GABA Antagonists/pharmacology
Glycine Agents/pharmacology
Neuronal Plasticity/physiology
Organ Culture Techniques
Rats
Receptors, AMPA/physiology
Receptors, GABA-A/physiology
Receptors, Glutamate/physiology
Receptors, Glycine/physiology
Receptors, Kainic Acid/physiology
Spinal Cord/cytology,drug effects,physiology
Strychnine/pharmacology
Synapses/drug effects,physiology
Tetrodotoxin/pharmacology
Time Factors
Chemicals
Drug Combinations
Excitatory Amino Acid Antagonists
GABA Antagonists
Glycine Agents
Receptors, AMPA
Receptors, GABA-A
Receptors, Glutamate
Receptors, Glycine
Receptors, Kainic Acid
Tetrodotoxin
6-Cyano-7-nitroquinoxaline-2,3-dione
Strychnine
Bicuculline
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Galante M
Biophysics Sector and Istituto Nazionale di Fisica della Materia Unit, International School for Advanced Studies (SISSA), via Beirut 4, 34014 Trieste, Italy.
[email protected]
Nistri A
Ballerini L
References (32)
32 references, click to expand
-
Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors.
Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7097-102
PMID: 9618545
-
Detection of spontaneous synaptic events with an optimally scaled template.
Biophys J. 1997 Jul;73(1):220-9
PMID: 9199786
-
An Organotypic Spinal Cord - Dorsal Root Ganglion - Skeletal Muscle Coculture of Embryonic Rat. II. Functional Evidence for the Formation of Spinal Reflex Arcs In Vitro.
Eur J Neurosci. 1991 Oct;3(11):1054-1068
PMID: 12106237
-
Regular oscillations of synaptic activity in spinal networks in vitro.
J Neurophysiol. 1993 Sep;70(3):871-8
PMID: 8229175
-
Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact.
J Neurosci. 1999 Apr 15;19(8):3007-22
PMID: 10191318
-
NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection.
J Neurosci. 1990 Apr;10(4):1197-216
PMID: 2158526
-
Activity-dependent modulation of synaptic AMPA receptor accumulation.
Neuron. 1998 Nov;21(5):1067-78
PMID: 9856462
-
The time courses of excitatory and inhibitory synaptic actions.
J Physiol. 1959 Mar 12;145(3):529-46
PMID: 13642318
-
The physiology of excitatory amino acids in the vertebrate central nervous system.
Prog Neurobiol. 1987;28(3):197-276
PMID: 2883706
-
Spontaneous correlated activity in developing neural circuits.
Neuron. 1999 Apr;22(4):653-6
PMID: 10230785
-
Glycine-receptor activation is required for receptor clustering in spinal neurons.
Nature. 1998 Apr 16;392(6677):717-20
PMID: 9565032
-
Selective up-regulation of an NMDA receptor subunit mRNA in cultured cerebellar granule cells by K(+)-induced depolarization and NMDA treatment.
Neuron. 1994 Jan;12(1):87-95
PMID: 8292362
-
Contribution of single-channel properties to the time course and amplitude variance of quantal glycine currents recorded in rat motoneurons.
J Neurophysiol. 1999 Apr;81(4):1608-16
PMID: 10200197
-
Network bursting by organotypic spinal slice cultures in the presence of bicuculline and/or strychnine is developmentally regulated.
Eur J Neurosci. 1998 Sep;10(9):2871-9
PMID: 9758156
-
Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons.
Neuron. 1993 Dec;11(6):1083-91
PMID: 7506044
-
Plasticity in the intrinsic excitability of cortical pyramidal neurons.
Nat Neurosci. 1999 Jun;2(6):515-20
PMID: 10448215
-
Neuronal activity during development: permissive or instructive?
Curr Opin Neurobiol. 1999 Feb;9(1):88-93
PMID: 10072369
-
Strychnine-sensitive stabilization of postsynaptic glycine receptor clusters.
J Cell Sci. 1998 Feb;111 ( Pt 3):335-45
PMID: 9427682
-
Generation of rhythmic patterns of activity by ventral interneurones in rat organotypic spinal slice culture.
J Physiol. 1999 Jun 1;517 ( Pt 2):459-75
PMID: 10332095
-
Blockade and recovery of spontaneous rhythmic activity after application of neurotransmitter antagonists to spinal networks of the chick embryo.
J Neurosci. 1998 Jan 1;18(1):294-306
PMID: 9412508
-
Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same.
Trends Neurosci. 1999 May;22(5):221-7
PMID: 10322495
-
An Organotypic Spinal Cord - Dorsal Root Ganglion - Skeletal Muscle Coculture of Embryonic Rat. I. The Morphological Correlates of the Spinal Reflex Arc.
Eur J Neurosci. 1991 Oct;3(11):1037-1053
PMID: 12106236
-
Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures.
Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11631-6
PMID: 10500228
-
Miniature excitatory postsynaptic potentials in embryonic motoneurons grown in slice cultures of spinal cord, dorsal root ganglia and skeletal muscle.
Exp Brain Res. 1992;89(2):453-8
PMID: 1623988
-
Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord.
J Neurophysiol. 1996 Feb;75(2):640-7
PMID: 8714641
-
A rise in postsynaptic Ca2+ potentiates miniature excitatory postsynaptic currents and AMPA responses in hippocampal neurons.
Neuron. 1994 Jan;12(1):127-38
PMID: 7507335
-
Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons.
Neuron. 1997 Oct;19(4):801-12
PMID: 9354327
-
Properties of spontaneous inhibitory synaptic currents in cultured rat spinal cord and medullary neurons.
J Neurophysiol. 1996 Jul;76(1):448-60
PMID: 8836236
-
Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude.
Neuron. 1997 Sep;19(3):697-709
PMID: 9331359
-
Impulse activity and the patterning of connections during CNS development.
Neuron. 1990 Dec;5(6):745-56
PMID: 2148486
-
Activity-dependent scaling of quantal amplitude in neocortical neurons.
Nature. 1998 Feb 26;391(6670):892-6
PMID: 9495341
-
Activity and synaptic receptor targeting: the long view.
Neuron. 1998 Sep;21(3):459-62
PMID: 9768832