Pervasive locking, saturation, asymmetric rate sensitivity and double-valuedness in crayfish stretch receptors

The correspondence between afferent discharges and sinusoidal length modulations (0.2--10 cps, under 10% of the natural length variations) was studied in isolated fast-adapting stretch receptor organs (FAO) of crayfish, largely using average displays of rate vs. length (or derivatives) along the cycle. Rate modulations were greatest during early cycles and then stabilized, an initial adjustment remindful of mechanical preconditioning. Responses to stimulation in the FAO, as in the slowly-adapting organs (SAO) and possibly other receptors, exhibit the following features, all striking because of their magnitude and ubiquity. i) A zig-zag overall afferent rate vs. stimulus frequency graph with positively and negatively sloped segments. This precludes the straightforward use of Bode plots. ii) Marked non-linearities as an obvious stimulus-response locking in the positively sloped segments, a double-valuedness with one rate while stretching and another while shortening, a lower-limit saturation with the receptor silent for more than half a cycle, and an asymmetric rate sensitivity. iii) Clear-cut discharge leads relative to the stimulus at low frequencies and lags at high ones. The FAO responds worse than the SAO to low frequencies, and better to high ones; it is locked 1-to-1 in a much broader range (e.g., 3--100 vs. 1--3 cps). All features were strongly frequency-dependent. With higher frequencies: i) the number of impulses per cycle fell from several to just one and finally to one every several cycles at higher values; ii) the two values of each length approached one another usually but not always; iii) the silent proportion of the cycle increased; and iv) the rate sensitivity changed. Each feature can arise in principle at any of the transduction stages from length to discharge: the mechanical transduction from length to dendritic deformation, an the encoder one from generator potentials to discharges are particularly likely candidates.