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.

Information Transmission in Cercal Giant Interneurons Is Unaffected by Axonal Conduction Noise

“…Our measurements of the transmission jitter were in general agreement with measurements from the sciatic nerve of frogs [9], as well as in proprioceptive afferents in crabs [38]. In contrast, the jitter we measured was much smaller than the ∼25% error rate over 2.7 mm of conduction measured in squid giant axons [12], but much higher than values predicted from models in that system, which were in the range of ∼0.02% error rate [15], [39].…”

“…Since the magnitude of transmission jitter is relatively larger in thin axons, we would also predict a greater decrease in information transfer in such axons, and vice versa in larger axons. Indeed, in the relatively large axons of proprioceptive afferents in crabs, it has been shown that transmission jitter has relatively little effect on information transfer in comparison with encoding jitter [38]. This underscores the fact that the impact of noise on information transfer is likely to be neuron-specific, with large-diameter axons likely to be less affected by propagation noise.…”

Consequences of Converting Graded to Action Potentials upon Neural Information Coding and Energy Efficiency

“…The highest information rate attained by the spiking neuron model was 235 bits/s, whereas the graded neuron model attained information rates of 2240 bits/s. Thus, the graded neuron model encodes almost an order of magnitude more information per second than the spiking neuron model, reproducing experimentally observed differences between graded and spiking neurons [5]–[8].…”

“…Consequently, spike trains can encode fewer states within a given time period than analogue voltage signals. This is borne out by experimental measurements that show the conversion of the graded generator potential into a spike train reduces the information rate [5]–[7]. Thus, non-spiking neurons that encode information as graded potentials typically have much higher information rates than spiking neurons [5],[8],[9].…”

Functional analysis of ultra high information rates conveyed by rat vibrissal primary afferents

“…To our knowledge, the highest published rate so far is that of photoreceptors of diurnal bees and mechanoreceptors of cockroaches, both of which reach about 500 bit/s, matching the information rate found here (French and Torkkeli, 1998; Frederiksen et al, 2008). Other sensory receptors and afferents have been reported to transfer less but still above 180 bit/s, amongst them frog and grass hopper auditory fibers (Rieke et al, 1995; Machens et al, 2001), cricket mechanosensory receptors (Roddey and Jacobs, 1996), chordodontal proprioceptive afferents of the shore crab (Dicaprio et al, 2007), and P-type electroreceptor afferents in electric fish (Wessel et al, 1996). Transfer ranges below 100 bit/s were observed in turtle vestibular canal afferents, and electroreceptor afferents of paddlefish (Neiman et al, 2011; Rowe and Neiman, 2012).…”