Journal of Neurophysiology, Vol 66, Issue 3 894-904, Copyright © 1991 by APS
Intracellular analysis of excitatory-inhibitory synaptic interactions in crayfish stretch receptors
L. C. Barrio, A. Araque, V. Abraira and W. Buno
Neurofisiologia, Instituto Cajal, Consejo Superior de Investigaciones Cientificas.
1. To determine the membrane mechanisms underlying the interactions between
inhibitory postsynaptic potentials (IPSPs) and excitatory inputs, we
investigated, at the membrane potential level, the combined influences of
low-frequency (0.05-0.50 Hz) imposed sinusoidal transmembrane currents
(termed sine currents), representing the excitatory drive, and trains of
regular (3-30/s) IPSPs. The two simplest possible neuron systems
exemplified by the slowly and rapidly adapting stretch receptors of
crayfish (RM1 and RM2, respectively) were used. 2. At constant elongation
the RM1 and RM2 behaved as a pacemaker and a neuron without self-sustained
oscillations, respectively, but in dynamic conditions uninhibited controls
and IPSP sine current interactions were essentially identical in both RMs.
Controls showed the usual smooth variation of the RM firing rate in
response to the gradually varying excitatory input. IPSP effects were
characterized by the expected overall reduction of the postsynaptic firing
rate. More important, special effects were also present, such as the simple
fixed alternations of IPSP and postsynaptic spikes (e.g., 1 IPSP, 1
postsynaptic or 1:1; 1 IPSP, 2 postsynaptic or 1:2; 2 IPSPs, 1 postsynaptic
spike or 2:1), where interspike intervals were more constant than
uninhibited controls and where the sensitivity to the excitatory input was
reduced to small values, and the sudden firing rate discontinuities
consisting of instantaneous discharge accelerations or decelerations
(termed "jumps") between successive alteration ratios, where sensitivity
increased to large values. Therefore with inhibition the RM firing rate
varied discontinuously in response to the gradually changing input, and the
discharge rate could take one of several discrete values by switching
between different alteration ratios. 3. At the alternations the times
elapsed between an IPSP and the closest spike before (phase, phi) or after
it (cophase, theta) increased and decreased, respectively, with increasing
excitation. The major membrane potential modification that accompanied the
interactions at the alternations was the gradual increase of the post-IPSP
slope as a function of excitatory drive, which reduced the time to reach
the firing level or theta. 4. Inhibition introduced subtle and complex
nonlinear modifications in the coding of convergent excitatory input. The
most notable nonlinearity was the discontinuous variations of the firing
rate as a function of the gradually changing excitatory input. Effects were
due to voltage interactions occurring at the extrasynaptic membrane, with a
decisive involvement of the spike generator and insignificant participation
of the shunting action of IPSPs. The results provide yet another example of
the predominant influence of intrinsic membrane properties in determining
the effects of synaptic-evoked activity.(ABSTRACT TRUNCATED AT 400 WORDS)
