Representation of sensory information in the cricket cercal sensory system. II. Information theoretic calculation of system accuracy and optimal tuning-curve widths of four primary interneurons

Abstract

1. Principles of information theory were used to calculate the limit of accuracy achievable by a subset of the wind-sensitive primary interneurons in the cricket cercal sensory system. For these calculations, an ensemble of four neurons was treated as an information channel, which encoded the direction of air-current stimuli for a defined range of air-current velocities. The specific information theoretic parameter that was calculated was the "transin-formation" or "mutual information" between the air-current directions and the neuronal spike trains, which were characterized in the preceding report. Under the assumptions used for these calculations, the ensemble of four interneurons was demonstrated to be capable of encoding between 4.2 and 3.5 bits of information about wind direction. This corresponds to an average directional accuracy of 4.7 and 7.7 degrees, respectively. 2. The same principles were applied to estimate the extent to which any variation in the width of the tuning curves would affect the transfer of information. As the widths of simulated tuning curves were varied, the mean ensemble accuracy showed a clear global maximum. This maximum corresponds to tuning curves widths of 110 degrees wide (at half maximum), which was remarkably close to the actual mean widths of the tuning curves observed in the cricket of 130 degrees. 3. The effect of varying the parametric "spacing" of the tuning curves within the stimulus range was also examined through a series of simulations. The configuration allowing the maximum information transfer corresponded to equal spacing of the tuning curves around the stimulus range (i.e., 90 degrees separation of peak sensitivity points). This theoretically optimum spacing corresponded exactly to the values observed in the experiments presented in the preceding report. 4. These simulations also showed that the degradation in the accuracy resulting from a shift in the tuning-curve spacing would depend on the plasticity of the higher order decoder of directional information. If there were no plasticity in the interneurons making up the higher order decoder, then the accuracy would be degraded by 50% for a mean tuning-curve shift of only 3.5 degrees. However, if the higher order decoding network were capable of being reoptimized to any arbitrary shift in tuning curves, the degradation in attainable accuracy would be much less severe as shifts of up to 10 degrees would result in virtually no degradation in the accuracy. 5. From these results, two general conclusions can be drawn about the coding of specific stimulus parameters by arrays of sensory cells.(ABSTRACT TRUNCATED AT 400 WORDS)