Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons.

1. The effects of small, brief depolarizing pulses and excitatory postsynaptic potentials (EPSPs) on neuronal firing were examined in layer V neurons in slices of cat sensorimotor cortex. During intracellular recording, brief depolarizing current pulses (duration, 0.5-2.0 ms; amplitude, 0.1-4.0 nA) were injected in neurons to produce pulse potentials (PPs) with a near-linear rise to a peak (0.08-3.6 mV; rise time = pulse duration) followed by an exponential decay. These PPs resembled EPSPs evoked by electrical stimulation of adjacent sites. When injected in neurons that were induced to discharge tonically, the PPs shortened the interspike intervals (ISIs) in two ways, depending on their time of arrival in the ISI. 2. Toward the end of the ISI, the PPs crossed a time-varying firing level, thereby directly evoking action potentials and shortening the ISIs. These directly evoked spikes occurred during the rise or peak of the PPs. The absolute firing level increased with the membrane trajectory during the latter part of the ISI. 3. PPs that appeared earlier in the ISI did not cross firing level directly but could nevertheless shorten the ISI by a slow regenerative process. The indirectly evoked spikes occurred after the peak of the PPs, at latencies whose magnitude and variability increased as the PPs appeared at successively earlier times in the ISI. PPs that occurred during the initial portion (approximately the 1st 3rd) of the ISI did not affect ISI duration. 4. Stimulus-evoked EPSPs shortened the ISIs in a manner similar to that of PPs. Like PPs, EPSPs caused direct crossings late in the ISI and indirect crossings earlier. Comparison of the mean and maximum ISI shortenings and the range of delays in which the PPs and EPSPs consistently produced ISI shortenings revealed no systematic differences. These similarities suggest that PPs may be used to simulate the ISI shortenings caused by EPSPs. 5. To characterize possible mechanisms underlying the ISI shortening, we examined the PP shapes at different times in the ISI. PPs immediately following a spike were smaller and decayed more rapidly than those evoked by the same current at rest. Late in the ISI, when the membrane potential was > 5 mV above rest, the PP height exceeded that of the PP at rest. This amplitude increase may be due to activation of the persistent sodium current.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  J. Eccles,et al.  The generation of impulses in motoneurones , 1957, The Journal of physiology.

[2]  M. Fuortes,et al.  STEPS IN THE PRODUCTION OF MOTONEURON SPIKES , 1957, The Journal of general physiology.

[3]  D. Kernell,et al.  Synaptic stimulation superimposed on motoneurones firing in the ‘secondary range’ to injected current , 1966, The Journal of physiology.

[4]  C. Stevens,et al.  Synaptic noise and other sources of randomness in motoneuron interspike intervals. , 1968, Journal of neurophysiology.

[5]  C. Stevens,et al.  Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma , 1971, The Journal of physiology.

[6]  P. Schwindt,et al.  Membrane-potential trajectories underlying motoneuron rhythmic firing at high rates. , 1973, Journal of neurophysiology.

[7]  P. Schwindt,et al.  Nature of conductances underlying rhythmic firing in cat spinal motoneurons. , 1973, Journal of neurophysiology.

[8]  B. Gustafsson Afterhyperpolarization and the control of repetitive firing in spinal neurones of the cat. , 1974, Acta physiologica Scandinavica. Supplementum.

[9]  W H Calvin,et al.  Three modes of repetitive firing and the role of threshold time course between spikes. , 1974, Brain research.

[10]  B. Walmsley,et al.  The effect of polarizing currents on unitary Ia excitatory post‐synaptic potentials evoked in spinal motoneurones. , 1976, The Journal of physiology.

[11]  W H Calvin,et al.  Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. , 1976, Journal of neurophysiology.

[12]  Michikazu Matsumura,et al.  Intracellular synaptic potentials of primate motor cortex neurons during voluntary movement , 1979, Brain Research.

[13]  P. Schwindt,et al.  Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. , 1982, Journal of neurophysiology.

[14]  E E Fetz,et al.  Relation between shapes of post‐synaptic potentials and changes in firing probability of cat motoneurones , 1983, The Journal of physiology.

[15]  P. Schwindt,et al.  Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[16]  P. Schwindt,et al.  Cable properties of layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[17]  P. Schwindt,et al.  Repetitive firing in layer V neurons from cat neocortex in vitro. , 1984, Journal of neurophysiology.

[18]  B. Gustafsson,et al.  Influence of stretch‐evoked synaptic potentials on firing probability of cat spinal motoneurones. , 1984, The Journal of physiology.

[19]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.

[20]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  P. Schwindt,et al.  Anomalous rectification in neurons from cat sensorimotor cortex in vitro. , 1987, Journal of neurophysiology.

[22]  E E Fetz,et al.  Cross‐correlation assessment of synaptic strength of single Ia fibre connections with triceps surae motoneurones in cats. , 1987, The Journal of physiology.

[23]  Y. Kang,et al.  Excitatory synaptic actions between pairs of neighboring pyramidal tract cells in the motor cortex. , 1988, Journal of neurophysiology.

[24]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[25]  P. Schwindt,et al.  Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. , 1988, Journal of neurophysiology.

[26]  E. Fetz,et al.  Intracortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex , 1988, Brain Research.

[27]  P. Schwindt,et al.  Influence of anomalous rectifier activation on afterhyperpolarizations of neurons from cat sensorimotor cortex in vitro. , 1988, Journal of neurophysiology.

[28]  A. Thomson,et al.  Voltage-dependent currents prolong single-axon postsynaptic potentials in layer III pyramidal neurons in rat neocortical slices. , 1988, Journal of neurophysiology.

[29]  R Porter,et al.  Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. , 1988, The Journal of physiology.

[30]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[31]  P. Schwindt,et al.  Two transient potassium currents in layer V pyramidal neurones from cat sensorimotor cortex. , 1991, The Journal of physiology.

[32]  A. Reyes,et al.  Effects of transient depolarizing potentials on the firing rate of cat neocortical neurons. , 1993, Journal of neurophysiology.