Refractory Sampling Links Efficiency and Costs of Sensory Encoding to Stimulus Statistics

Abstract

Sensory neurons integrate information about the world, adapting their sampling to its changes. However, little is understood mechanistically how this primary encoding process, which ultimately limits perception, depends upon stimulus statistics. Here, we analyze this open question systematically by using intracellular recordings from fly (Drosophila melanogaster and Coenosia attenuata) photoreceptors and corresponding stochastic simulations from biophysically realistic photoreceptor models. Recordings show that photoreceptors can sample more information from naturalistic light intensity time series (NS) than from Gaussian white-noise (GWN), shuffled-NS or Gaussian-1/f stimuli; integrating larger responses with higher signal-to-noise ratio and encoding efficiency to large bursty contrast changes. Simulations reveal how a photoreceptor's information capture depends critically upon the stochastic refractoriness of its 30,000 sampling units (microvilli). In daylight, refractoriness sacrifices sensitivity to enhance intensity changes in neural image representations, with more and faster microvilli improving encoding. But for GWN and other stimuli, which lack longer dark contrasts of real-world intensity changes that reduce microvilli refractoriness, these performance gains are submaximal and energetically costly. These results provide mechanistic reasons why information sampling is more efficient for natural/naturalistic stimulation and novel insight into the operation, design, and evolution of signaling and code in sensory neurons.

Electrophysiological Method for Recording Intracellular Voltage Responses of <em>Drosophila</em> Photoreceptors and Interneurons to Light Stimuli <em>In Vivo</em>

“…The system has the most complete wiring diagram 1,2 and is amiable to genetic manipulations and accurate neural activity monitoring (of high signal-to-noise ratio and time-resolution) [3][4][5][6][7][8][9][10] .…”

“…The eye's primary information sampling units are its rhabdomeric photoreceptors 7,8,11 . Each ommatidium contains eight photoreceptor cells (R1-R8), which share the same facet lens but are aligned to seven different directions.…”

“…Finally, axonal gap-junctions, linking neighboring R1-R6 and between R6 and R7/R8 photoreceptors in the lamina, contribute to the asymmetric information representation and processing in each cartridge 14,20,28 . Intracellular voltage recordings from individual photoreceptors and visual interneurons in nearly intact Drosophila provide high signal-to-noise ratio data at sub-millisecond resolution 3,5,[7][8][9][10]29 -100 msec resolution. Furthermore, because the electrodes have very small and sharp tips, the method is not restricted to cell bodies, but can provide direct recordings from small active neural structures; such as the LMCs' dendritic trees or photoreceptor axons, which cannot be accessed by much larger tips of patch-clamp electrodes.…”

“…Importantly, the method is also structurally less invasive and damaging than most patch-clamp applications, and so affects less the studied cells' intracellular milieu and information sampling. Thus, conventional sharp microelectrode techniques have contributed, and keep on contributing, fundamental discoveries and original insight into neural information processing at the appropriate time scale; improving our mechanistic understanding of vision [3][4][5][6][7][8][9][10] . This article explains how in vivo intracellular recordings from Drosophila R1-R6 photoreceptors and LMCs are performed in the Juusola laboratory.…”

Vision in dim light: highlights and challenges

“…This 'transducer noise' originates in the biochemical enzyme cascades responsible for the massive signal amplification required to change ion fluxes enough for the photoreceptor voltage response to give a reliable response to single photons [38 -40]. Although this transducer noise has the potential to degrade the reliability of vision, some recent work suggests it could, remarkably, have the opposite effect [41,42]. Secondly, as first predicted by Horace Barlow almost 60 years ago [43], and confirmed two decades later in toad rods [36], the biochemical pathways responsible for transduction are occasionally activated even in perfect darkness.…”