Participation of voltage-gated conductances on the response succeeding inhibitory synaptic potentials in the crayfish slowly adapting stretch receptor neuron

L. C. Barrio, A. Araque, W. Buno

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Abstract

1. We examined the contribution of voltage-gated conductances to inhibitory postsynaptic potential (IPSP) effects under current clamp in silent and spiking slowly adapting stretch receptor neurons (SN1s) in the slow receptor muscle of the crayfish Procambarus. The receptor exemplifies the simplest inhibitory neural circuit, with one presynaptic and one postsynaptic neuron. The effects of synaptic inhibition were compared with the outcome of hyperpolarizing current pulses. Because pulse effects were exclusively due to postsynaptic mechanisms, an estimation of the synaptic or extrasynaptic origin of the results of IPSP was possible. 2. Inhibition by single IPSPs increased gradually with the time elapsed from the preceding spike in 60% of the spiking SN1s. However, early IPSP arrivals were exclusively excitatory in the rest of the cases. Inhibition was restricted to a single expanded SN1 interspike interval, but the early excitation and the postinhibitory rebound lasted several intervals. Rebound was invariably present; it was the only consequence of IPSPs in silent receptors and could be extremely long lasting (>25 s). 3. The membrane potential of the SN1 neuron was clamped at hyperpolarized values (greater than -65 mV) by prolonged IPSP barrages at high rate (>20/s). A prominent depolarizing sag and a gradual reduction of the IPSP amplitude were observed with prolonged presynaptic stimulation. There were subthreshold IPSP amplitude oscillations consisting of gradual increases and decreases of the post-IPSP peak depolarization at lower presynaptic rates. IPSP amplitude variations (≤10 mV) were primarily due to larger local responses. 4. Essentially all IPSP effects were mimicked by hyperpolarizing pulses. Sag was also evoked by pulses and was accompanied by a gradual conductance increase preceded by a brief initial drop. Sag and rebound were markedly reduced by Cs+ (2 mM) and tetrodotoxin (1 μM) and less by Ba2+ (5 mM) or tetraethylammonium (25 mM) superfusion. Both were somewhat decreased by acetylcholine (30 μM), which also markedly depolarized and accelerated firings, results which were usually reduced by atropine (10 μM). 5. In conclusion, IPSP and hyperpolarizing pulse effects were essentially identical, implying that extrasynaptic membrane properties were decisive. Interestingly, net excitatory consequences were usual, effectively increasing sensitivity and reducing the sensory threshold. Pharmacological evidence is provided suggesting that the hyperpolarization-activated current, I(Q), and also probably the K+ M- current, the A-current, and the low-threshold, persistent Na+ conductances participate in sag and rebound genesis. A mathematical model including all the above conductances displayed most of the naturally occurring behaviors, suggesting that the assumptions regarding the underlying membrane mechanisms were sound.

Original languageEnglish (US)
Pages (from-to)1140-1151
Number of pages12
JournalJournal of neurophysiology
Volume72
Issue number3
DOIs
StatePublished - Jan 1 1994
Externally publishedYes

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