Dynamic analysis of sensory-inhibitory interactions in crayfish stretch receptor neurons

1. The effects of regular and random inhibition at moderate rates on the sensory response evoked by sinusoidal stretches were investigated in slowly and rapidly adapting stretch receptors of crayfish (RM1 and RM2, respectively). 2. Although the RM1 has pacemaker properties and the RM2 is spontaneously silent, inhibitory postsynaptic potential (IPSP) effects were similar in both mechanosensory neurons. The most common consequence was the expected reduction of the sensory response and the increase of the elongation needed to reach firing threshold. With regular IPSPs there were regions where pre- and postsynaptic spikes alternated at fixed integer ratios, usually 1:1, more rarely 1:2 and 1:3. Increases or decreases of the sensory excitation caused sudden postsynaptic accelerations or decelerations when specific length bounds were crossed and where pre- and postsynaptic alternations changed to lower (e.g., from 1:1 to 1:2) or higher ratios (e.g., from 1:2 to 1:1), respectively. 3. Paradoxical effects were also observed because increasing or decreasing the inhibitory rate for a given alternation ratio (e.g., 1:1) accelerated or decelerated the output rate, respectively. Alternations and paradoxical behaviors disappeared with IPSP pattern irregularization. Random IPSPs strongly irregularized the receptor's output. Inhibition, especially if the pattern was irregular, could excite under special conditions. 4. With regular IPSPs, mechanical sensitivity became zero at the lengths at which receptors were silenced, low during alternations, and maximum at transitions between successive alternation ratios. Irregular IPSPs did not have this delinearizing consequence. 5. In conclusion, inhibition introduced important complex modifications in the coding of mechanosensory information. Effects were similar in both receptor types, indicating that self-sustained oscillations are not fundamental. The observed changes were critically dependent on pre- and postsynaptic rate and pattern. They cannot be explained by simple summation of converging sensory and inhibitory inputs and represent another observation of the complex dynamic behavior of periodically driven nonlinear systems.