Information Rate and Spike-Timing Precision of Proprioceptive Afferents

Abstract

Proprioception in the first two joints of crustacean limbs is mediated by chordotonal organs that utilize spike-mediated information coding and transmission and by nonspiking proprioceptive afferents that use graded transmission at information rates in excess of 2,500 bits/s. Chordotonal organs operate in parallel with the graded receptors, but the information rates of the spiking chordotonal afferents have not been previously determined. Lower-bound estimates of chordotonal afferent information rates were calculated using stimulus reconstruction, which assumes linear encoding of the stimulus. The information rate was also directly estimated from the spike train entropy, which makes no a priori assumptions with respect to the coding scheme used by the system. Lower-bound information rate estimates ranged from 43 to 69 bits/s, whereas the direct estimates ranged from 24 to 278 bits/s. Comparison of both estimates derived from the same data set indicates that a linear decoder could recover an average of 59% of the information from the spike train. Afferent spike timing was found to be extremely precise, with spikes evoked with an average timing jitter of 0.55 ms. Information rate was correlated with the mean jitter and the noise entropy of the spike train could be predicted from the mean firing rate and mean jitter. Direct stimulation of single afferents by current injection into the soma revealed that the average timing jitter was <0.1 ms, indicating that intrinsic membrane properties, spike generation, and mechanotransduction mechanisms are the major sources of timing jitter in this system.