A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis

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Abstract

1. The activation of current-clamped neurons in the chick nucleus magnocellularis (nMAG) by eighth nerve stimulation has been studied in a brain slice preparation using patch electrodes. Single presynaptic stimuli produced rapidly rising, suprathreshold, excitatory postsynaptic potentials (EPSPs) with a synaptic delay of ~0.4 ms. Spontaneous, miniature EPSPs (mEPSPs) were evident in control extracellular solution and in the presence of tetrodotoxin (TTX). 2. The EPSP was composed of a large, brief component that was sensitive to antagonists of α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptors, and a smaller, slowly decaying component that was sensitive to both N-methyl-D-aspartate (NMDA) and AMPA receptor antagonists. 3. Injection of depolarizing current steps revealed a strong outward rectification of the membrane conductance at potentials close to the resting potential. Consequently, neurons could fire only a single, TTX-sensitive action potential during a current step. The conductance responsible for this rectification was sensitive to 1 mM 4-aminopyridine but not to 1 mM tetraethylammonium. 4. Following the termination of depolarizing current pulses, membrane potential decayed with a half-time (t( 1/2 )) that decreased as the depolarizing current increased, reaching ~0.25 ms for a depolarization from rest of 20 mV. The t( 1/2 ) for the decay of EPSPs matched the membrane t( 1/2 ), indicating that the underlying synaptic conductance decays more quickly than the membrane t( 1/2 ). 5. The slow phase of the EPSP was always longer than the membrane t( 1/2 ) and increased in size with hyperpolarization. This result is consistent with the contribution of AMPA receptors to the slow, as well as fast, EPSP. 6. The safety factor for transmission with low-frequency stimuli was large, as indicated by the rise time of the EPSP, the extent to which the EPSP shunted the action potential, and the size of EPSPs after prolongation of the synaptic conductance by cyclothiazide. 7. During repetitive synaptic stimulation, the slow EPSPs summated to produce a plateau depolarization of 10-20 mV. The plateau potential was only partially blocked by NMDA receptor antagonists. 8. During trains of stimuli, the faster EPSPs rode atop the plateau potential and could drive action potentials at rates up to 500 Hz for short periods. Synaptic depression was evident during trains, such that EPSPs often fell below threshold after 5-10 stimuli at rates above 200 Hz. EPSPs could remain suprathreshold for several seconds at 50 Hz. 9. Synaptic jitter, measured as the standard deviation in the timing of the peak of the orthodromic spike, was 18 μs for low-frequency (≤1 Hz) stimuli. The jitter increased to ~40 μs for trains of suprathreshold responses at 10 Hz. At higher stimulus rates, the jitter and the response latency gradually increased during the train. 10. In some cells, a small EPSP occurred immediately after an action potential in the postsynaptic cell. This apparently autaptic input may result from an axonal collateral within the nucleus magnocellularis. 11. The high precision of transmission of auditory nerve signals into the cochlear nucleus of the chick involves the convergence of several physiological adaptations, including a brief membrane and synaptic current time constant and a very large synaptic drive. The summation of small, slow synaptic potentials provides a further mechanism for shortening the membrane time constant during repetitive synaptic activity.

Original languageEnglish (US)
Pages (from-to)705-718
Number of pages14
JournalJournal of Neurophysiology
Volume72
Issue number2
StatePublished - 1994
Externally publishedYes

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Excitatory Postsynaptic Potentials
Action Potentials
AMPA Receptors
Membranes
Tetrodotoxin
N-Methyl-D-Aspartate Receptors
Membrane Potentials
Miniature Postsynaptic Potentials
Physiological Adaptation
Cochlear Nucleus
Neurons
Synaptic Membranes
4-Aminopyridine
Cochlear Nerve
Synaptic Potentials
Tetraethylammonium
Reaction Time
Electrodes

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. / Zhang, S.; Trussell, Laurence.

In: Journal of Neurophysiology, Vol. 72, No. 2, 1994, p. 705-718.

Research output: Contribution to journalArticle

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N2 - 1. The activation of current-clamped neurons in the chick nucleus magnocellularis (nMAG) by eighth nerve stimulation has been studied in a brain slice preparation using patch electrodes. Single presynaptic stimuli produced rapidly rising, suprathreshold, excitatory postsynaptic potentials (EPSPs) with a synaptic delay of ~0.4 ms. Spontaneous, miniature EPSPs (mEPSPs) were evident in control extracellular solution and in the presence of tetrodotoxin (TTX). 2. The EPSP was composed of a large, brief component that was sensitive to antagonists of α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptors, and a smaller, slowly decaying component that was sensitive to both N-methyl-D-aspartate (NMDA) and AMPA receptor antagonists. 3. Injection of depolarizing current steps revealed a strong outward rectification of the membrane conductance at potentials close to the resting potential. Consequently, neurons could fire only a single, TTX-sensitive action potential during a current step. The conductance responsible for this rectification was sensitive to 1 mM 4-aminopyridine but not to 1 mM tetraethylammonium. 4. Following the termination of depolarizing current pulses, membrane potential decayed with a half-time (t( 1/2 )) that decreased as the depolarizing current increased, reaching ~0.25 ms for a depolarization from rest of 20 mV. The t( 1/2 ) for the decay of EPSPs matched the membrane t( 1/2 ), indicating that the underlying synaptic conductance decays more quickly than the membrane t( 1/2 ). 5. The slow phase of the EPSP was always longer than the membrane t( 1/2 ) and increased in size with hyperpolarization. This result is consistent with the contribution of AMPA receptors to the slow, as well as fast, EPSP. 6. The safety factor for transmission with low-frequency stimuli was large, as indicated by the rise time of the EPSP, the extent to which the EPSP shunted the action potential, and the size of EPSPs after prolongation of the synaptic conductance by cyclothiazide. 7. During repetitive synaptic stimulation, the slow EPSPs summated to produce a plateau depolarization of 10-20 mV. The plateau potential was only partially blocked by NMDA receptor antagonists. 8. During trains of stimuli, the faster EPSPs rode atop the plateau potential and could drive action potentials at rates up to 500 Hz for short periods. Synaptic depression was evident during trains, such that EPSPs often fell below threshold after 5-10 stimuli at rates above 200 Hz. EPSPs could remain suprathreshold for several seconds at 50 Hz. 9. Synaptic jitter, measured as the standard deviation in the timing of the peak of the orthodromic spike, was 18 μs for low-frequency (≤1 Hz) stimuli. The jitter increased to ~40 μs for trains of suprathreshold responses at 10 Hz. At higher stimulus rates, the jitter and the response latency gradually increased during the train. 10. In some cells, a small EPSP occurred immediately after an action potential in the postsynaptic cell. This apparently autaptic input may result from an axonal collateral within the nucleus magnocellularis. 11. The high precision of transmission of auditory nerve signals into the cochlear nucleus of the chick involves the convergence of several physiological adaptations, including a brief membrane and synaptic current time constant and a very large synaptic drive. The summation of small, slow synaptic potentials provides a further mechanism for shortening the membrane time constant during repetitive synaptic activity.

AB - 1. The activation of current-clamped neurons in the chick nucleus magnocellularis (nMAG) by eighth nerve stimulation has been studied in a brain slice preparation using patch electrodes. Single presynaptic stimuli produced rapidly rising, suprathreshold, excitatory postsynaptic potentials (EPSPs) with a synaptic delay of ~0.4 ms. Spontaneous, miniature EPSPs (mEPSPs) were evident in control extracellular solution and in the presence of tetrodotoxin (TTX). 2. The EPSP was composed of a large, brief component that was sensitive to antagonists of α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptors, and a smaller, slowly decaying component that was sensitive to both N-methyl-D-aspartate (NMDA) and AMPA receptor antagonists. 3. Injection of depolarizing current steps revealed a strong outward rectification of the membrane conductance at potentials close to the resting potential. Consequently, neurons could fire only a single, TTX-sensitive action potential during a current step. The conductance responsible for this rectification was sensitive to 1 mM 4-aminopyridine but not to 1 mM tetraethylammonium. 4. Following the termination of depolarizing current pulses, membrane potential decayed with a half-time (t( 1/2 )) that decreased as the depolarizing current increased, reaching ~0.25 ms for a depolarization from rest of 20 mV. The t( 1/2 ) for the decay of EPSPs matched the membrane t( 1/2 ), indicating that the underlying synaptic conductance decays more quickly than the membrane t( 1/2 ). 5. The slow phase of the EPSP was always longer than the membrane t( 1/2 ) and increased in size with hyperpolarization. This result is consistent with the contribution of AMPA receptors to the slow, as well as fast, EPSP. 6. The safety factor for transmission with low-frequency stimuli was large, as indicated by the rise time of the EPSP, the extent to which the EPSP shunted the action potential, and the size of EPSPs after prolongation of the synaptic conductance by cyclothiazide. 7. During repetitive synaptic stimulation, the slow EPSPs summated to produce a plateau depolarization of 10-20 mV. The plateau potential was only partially blocked by NMDA receptor antagonists. 8. During trains of stimuli, the faster EPSPs rode atop the plateau potential and could drive action potentials at rates up to 500 Hz for short periods. Synaptic depression was evident during trains, such that EPSPs often fell below threshold after 5-10 stimuli at rates above 200 Hz. EPSPs could remain suprathreshold for several seconds at 50 Hz. 9. Synaptic jitter, measured as the standard deviation in the timing of the peak of the orthodromic spike, was 18 μs for low-frequency (≤1 Hz) stimuli. The jitter increased to ~40 μs for trains of suprathreshold responses at 10 Hz. At higher stimulus rates, the jitter and the response latency gradually increased during the train. 10. In some cells, a small EPSP occurred immediately after an action potential in the postsynaptic cell. This apparently autaptic input may result from an axonal collateral within the nucleus magnocellularis. 11. The high precision of transmission of auditory nerve signals into the cochlear nucleus of the chick involves the convergence of several physiological adaptations, including a brief membrane and synaptic current time constant and a very large synaptic drive. The summation of small, slow synaptic potentials provides a further mechanism for shortening the membrane time constant during repetitive synaptic activity.

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