Abstract
Sensory receptors determine the type and the quantity of information available for perception. Here, we quantified and characterized the information transferred by primary afferents in the rat whisker system using neural system identification. Quantification of “how much” information is conveyed by primary afferents, using the direct method (DM), a classical information theoretic tool, revealed that primary afferents transfer huge amounts of information (up to 529 bits/s). Information theoretic analysis of instantaneous spike-triggered kinematic stimulus features was used to gain functional insight on “what” is coded by primary afferents. Amongst the kinematic variables tested—position, velocity, and acceleration—primary afferent spikes encoded velocity best. The other two variables contributed to information transfer, but only if combined with velocity. We further revealed three additional characteristics that play a role in information transfer by primary afferents. Firstly, primary afferent spikes show preference for well separated multiple stimuli (i.e., well separated sets of combinations of the three instantaneous kinematic variables). Secondly, neurons are sensitive to short strips of the stimulus trajectory (up to 10 ms pre-spike time), and thirdly, they show spike patterns (precise doublet and triplet spiking). In order to deal with these complexities, we used a flexible probabilistic neuron model fitting mixtures of Gaussians to the spike triggered stimulus distributions, which quantitatively captured the contribution of the mentioned features and allowed us to achieve a full functional analysis of the total information rate indicated by the DM. We found that instantaneous position, velocity, and acceleration explained about 50% of the total information rate. Adding a 10 ms pre-spike interval of stimulus trajectory achieved 80–90%. The final 10–20% were found to be due to non-linear coding by spike bursts.
Highlights
Primary afferents of the rodent whisker-related tactile system are classically categorized by their response pattern to rampand-hold stimuli (Gibson and Welker, 1983a,b)
In order to deal with these complexities, we used a flexible probabilistic neuron model fitting mixtures of Gaussians to the spike triggered stimulus distributions, which quantitatively captured the contribution of the mentioned features and allowed us to achieve a full functional analysis of the total information rate indicated by the direct method (DM)
The literature entails a multitude of studies measuring information rates and precision, sometimes employing the DM, but most commonly using stimulus reconstruction methods (Bialek et al, 1991)
Summary
Primary afferents of the rodent whisker-related tactile system are classically categorized by their response pattern to rampand-hold stimuli (Gibson and Welker, 1983a,b). Dynamic velocity ranges for SA and RA afferents seem to be complementary, with SA spiking best representing low velocities (750◦/s; Shoykhet et al, 2000; Stüttgen et al, 2006) While this notion is supported by studies using step-like stimuli (Stüttgen et al, 2006, 2008) it does not seem to apply in case of more complex stimuli (Jones et al, 2004a,b): Low-pass filtered white-noise stimuli activate both classes of primary afferents in an utmost precise way. Spike-triggered averages [or the related filter kernels that transform stimuli into spike trains, (Bialek et al, 1991)] computed from primary afferent responses to white-noise stimuli exhibit shapes that in most cases could not be described as uniquely encoding either position, velocity, or acceleration (Jones et al, 2004a). Spike-triggered averages differ according to the frequency range of the white-noise stimuli, suggesting more
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