GABAergic Excitation of Spider Mechanoreceptors Increases Information Capacity by Increasing Entropy Rather than Decreasing Jitter

Abstract

Neurotransmitter chemicals excite or inhibit a range of sensory afferents and sensory pathways. These changes in firing rate or static sensitivity can also be associated with changes in dynamic sensitivity or membrane noise and thus action potential timing. We measured action potential firing produced by random mechanical stimulation of spider mechanoreceptor neurons during long-duration excitation by the GABA A agonist muscimol. Information capacity was estimated from signal-to-noise ratio by averaging responses to repeated identical stimulation sequences. Information capacity was also estimated from the coherence function between input and output signals. Entropy rate was estimated by a data compression algorithm and maximum entropy rate from the firing rate. Action potential timing variability, or jitter, was measured as normalized interspike interval distance. Muscimol increased firing rate, information capacity, and entropy rate, but jitter was unchanged. We compared these data with the effects of increasing firing rate by current injection. Our results indicate that the major increase in information capacity by neurotransmitter action arose from the increased entropy rate produced by increased firing rate, not from reduction in membrane noise and action potential jitter.

Measuring entropy in continuous and digitally filtered neural signals

“…In contrast, action potential entropy was less than 10% of the input value. These data reflect the very low inherent noise level and wide frequency response function of the receptor potential in VS-3 neurons, as reported previously (Pfeiffer and French, 2009). …”

“…Details of the preparation for recording receptor potential and action potentials from spider mechanoreceptors have been described in detail before (Pfeiffer and French, 2009) and will only be briefly summarized here. Legs of adult spiders, Cupiennius salei, were autotomized following a protocol approved by the Dalhousie University Committee on Laboratory Animals.…”

“…One approach to neural information measurement is via signal-tonoise ratio, which provides an estimate of information capacity, the amount of information that could theoretically be carried by a noisy communication channel (Shannon and Weaver, 1949). This has the advantage that some methods of estimating signal-to-noise can be applied to both analog and digital signals (Juusola and French, 1997;Borst and Theunissen, 1999;Pfeiffer and French, 2009), providing valid comparisons.…”

Static and Dynamic Adaptation of Insect Photoreceptor Responses to Naturalistic Stimuli

“…More recent work has considered nonlinear effects on sensory information transmission in several sensory receptors, using naturalistic stimuli that approximate the natural range of amplitude distributions and dynamics (van der Schaaf and van Hateren, 1996; Juusola and de Polavieja, 2003; Niven et al, 2004). Accompanying this development has been a change of emphasis from communication channel information capacity (Shannon and Weaver, 1949) to nonlinear measurements of signal information based on entropy, as estimated from probability distributions (Juusola and de Polavieja, 2003; Takalo et al, 2011) or by data compression (Pfeiffer and French, 2009). …”

Synaptic transmission of graded membrane potential changes and spikes between identified visual interneurons

“…Our study is, to our knowledge, the first using VCcCC to manipulate the responses of neurons to sensory stimuli for the investigation of synaptic transmission to their postsynaptic targets. Previously, VCcCC was used during sensory stimulation of spider mechanoreceptor neurons to test whether modulatory GABAergic inputs to the neurons exert their specific effects on firing rate and information coding via changes in conductance or changes in membrane potential (Pfeiffer & French, 2009; Pfeiffer et al. , 2009).…”