Fly Photoreceptors Demonstrate Energy-Information Trade-Offs in Neural Coding

Trade-offs between energy consumption and neuronal performance must shape the design and evolution of nervous systems, but we lack empirical data showing how neuronal energy costs vary according to performance. Using intracellular recordings from the intact retinas of four flies, Drosophila melanogaster, D. virilis, Calliphora vicina, and Sarcophaga carnaria, we measured the rates at which homologous R1–6 photoreceptors of these species transmit information from the same stimuli and estimated the energy they consumed. In all species, both information rate and energy consumption increase with light intensity. Energy consumption rises from a baseline, the energy required to maintain the dark resting potential. This substantial fixed cost, ∼20% of a photoreceptor's maximum consumption, causes the unit cost of information (ATP molecules hydrolysed per bit) to fall as information rate increases. The highest information rates, achieved at bright daylight levels, differed according to species, from ∼200 bits s(−1) in D. melanogaster to ∼1,000 bits s(−1) in S. carnaria. Comparing species, the fixed cost, the total cost of signalling, and the unit cost (cost per bit) all increase with a photoreceptor's highest information rate to make information more expensive in higher performance cells. This law of diminishing returns promotes the evolution of economical structures by severely penalising overcapacity. Similar relationships could influence the function and design of many neurons because they are subject to similar biophysical constraints on information throughput

Optimizing the use of a sensor resource for opponent polarization coding

Flies use specialized photoreceptors R7 and R8 in the dorsal rim area (DRA) to detect skylight polarization. R7 and R8 form a tiered waveguide (central rhabdomere pair, CRP) with R7 on top, filtering light delivered to R8. We examine how the division of a given resource, CRP length, between R7 and R8 affects their ability to code polarization angle. We model optical absorption to show how the length fractions allotted to R7 and R8 determine the rates at which they transduce photons, and correct these rates for transduction unit saturation. The rates give polarization signal and photon noise in R7, and in R8. Their signals are combined in an opponent unit, intrinsic noise added, and the unit’s output analysed to extract two measures of coding ability, number of discriminable polarization angles and mutual information. A very long R7 maximizes opponent signal amplitude, but codes inefficiently due to photon noise in the very short R8. Discriminability and mutual information are optimized by maximizing signal to noise ratio, SNR. At lower light levels approximately equal lengths of R7 and R8 are optimal because photon noise dominates. At higher light levels intrinsic noise comes to dominate and a shorter R8 is optimum. The optimum R8 length fractions falls to one third. This intensity dependent range of optimal length fractions corresponds to the range observed in different fly species and is not affected by transduction unit saturation. We conclude that a limited resource, rhabdom length, can be divided between two polarization sensors, R7 and R8, to optimize opponent coding. We also find that coding ability increases sub-linearly with total rhabdom length, according to the law of diminishing returns. Consequently, the specialized shorter central rhabdom in the DRA codes polarization twice as efficiently with respect to rhabdom length than the longer rhabdom used in the rest of the eye.Simon Laughlin is supported by an honorarium from H. Britton Sanderford. Francisco Heras was supported by grants from Fundación Caja, Madrid; Trinity College, Cambridge; and the Departmentt of Zoology, University of Cambridge

Neuronal energy consumption: biophysics, efficiency and evolution

Electrical and chemical signaling within and between neurons consumes energy. Recent studies have sought to refine our understanding of the processes that consume energy and their relationship to information processing by coupling experiments with computational models and energy budgets. These studies have produced insights into both how neurons and neural circuits function, and why they evolved to function in the way they do

A neurobiological and computational analysis of target discrimination in visual clutter by the insect visual system.

Some insects have the capability to detect and track small moving objects, often against cluttered moving backgrounds. Determining how this task is performed is an intriguing challenge, both from a physiological and computational perspective. Previous research has characterized higher-order neurons within the fly brain known as 'small target motion detectors‘ (STMD) that respond selectively to targets, even within complex moving surrounds. Interestingly, these cells still respond robustly when the velocity of the target is matched to the velocity of the background (i.e. with no relative motion cues). We performed intracellular recordings from intermediate-order neurons in the fly visual system (the medulla). These full-wave rectifying, transient cells (RTC) reveal independent adaptation to luminance changes of opposite signs (suggesting separate 'on‘ and 'off‘ channels) and fast adaptive temporal mechanisms (as seen in some previously described cell types). We show, via electrophysiological experiments, that the RTC is temporally responsive to rapidly changing stimuli and is well suited to serving an important function in a proposed target-detecting pathway. To model this target discrimination, we use high dynamic range (HDR) natural images to represent 'real-world‘ luminance values that serve as inputs to a biomimetic representation of photoreceptor processing. Adaptive spatiotemporal high-pass filtering (1st-order interneurons) shapes the transient 'edge-like‘ responses, useful for feature discrimination. Following this, a model for the RTC implements a nonlinear facilitation between the rapidly adapting, and independent polarity contrast channels, each with centre-surround antagonism. The recombination of the channels results in increased discrimination of small targets, of approximately the size of a single pixel, without the need for relative motion cues. This method of feature discrimination contrasts with traditional target and background motion-field computations. We show that our RTC-based target detection model is well matched to properties described for the higher-order STMD neurons, such as contrast sensitivity, height tuning and velocity tuning. The model output shows that the spatiotemporal profile of small targets is sufficiently rare within natural scene imagery to allow our highly nonlinear 'matched filter‘ to successfully detect many targets from the background. The model produces robust target discrimination across a biologically plausible range of target sizes and a range of velocities. We show that the model for small target motion detection is highly correlated to the velocity of the stimulus but not other background statistics, such as local brightness or local contrast, which normally influence target detection tasks. From an engineering perspective, we examine model elaborations for improved target discrimination via inhibitory interactions from correlation-type motion detectors, using a form of antagonism between our feature correlator and the more typical motion correlator. We also observe that a changing optimal threshold is highly correlated to the value of observer ego-motion. We present an elaborated target detection model that allows for implementation of a static optimal threshold, by scaling the target discrimination mechanism with a model-derived velocity estimation of ego-motion. Finally, we investigate the physiological relevance of this target discrimination model. We show that via very subtle image manipulation of the visual stimulus, our model accurately predicts dramatic changes in observed electrophysiological responses from STMD neurons.Thesis (Ph.D.) - University of Adelaide, School of Molecular and Biomedical Science, 200

AN INVESTIGATION OF THE PHOTOTRANSDUCTION CASCADE AND TEMPORAL CHARACTERISTICS OF THE RETINA OF THE CUTTLEFISH, SEPIA OFFICINALIS

Cephalopods have extremely well developed visual systems which are of particular interest due to the well known morphological similarity of the cephalopod eye to the vertebrate eye. This similarity ends at the level of the photoreceptors where vertebrates and invertebrates have been found to use different intracellular second messengers. Although the effect of extracellular ion manipulation on the light response has been examined and some very useful biochemical studies carried out, the pathway has not been investigated by the use of pharmacological intervention; a method which has proved to be useful in other preparations. This study examines various properties of the photoreceptors of the cuttlefish, Sepia officinalis, with particular interest in the second messenger signalling pathway. Both extracellular and whole cell patch clamp recording has been utilised. The second messenger signalling pathway, which mediates phototransduction in the retina of S. officinalis, was investigated by recording the electroretinogram and examining how this changed with the application of various extracellularly applied, membrane permeable pharmacological agents. Invertebrate phototransduction utilises the phosphoinositide (PI) signalling pathway therefore specific activators and inhibitors targeted at precise sites of this pathway were applied to the extracellular bathing solution. These studies indicated that cleavage of phosphatidylinositol-4,5-bisphosphate is essential for the production of a light response and that the inositol trisphophate (IP3) branch of this pathway is of greatest importance in this preparation, as opposed to the diacylglycerol branch. How this second messenger cascade transfers the incoming information into a temporally coded signal was studied by measuring maximum critical flicker fusion frequency. The effect of cell size on this property was investigated and also how cell sensitivity was affected and whether these properties appeared to fit the animal's environmental conditions or whether they were restricted by cellular properties. The animals were found to have relatively "slow" eyes. However the younger age group studied, with shorter photoreceptors, was found to be both faster and more sensitive. This was an unexpected finding considering temporal resolving power is often sacrificed for sensitivity. It is suggested that the observed differences between age groups was attributable to the effects of increased cell size on the cell membrane time constant and that deterioration of signalling molecules with aging may also be a contributing factor. An investigation of the cell signalling pathway at the level of individual cells was also carried out using the whole cell patch clamp technique. Using this technique, two voltage activated currents were found; an inward sodium current characterised by its voltage and tetrodotoxin sensitivity, and an outward potassium current characterised by its tetraethylammonium sensitivity. As well as finding further evidence for the involvement of the IP3 branch of the PI pathway there is also evidence of a role for cyclic guanosine monophosphate. A suitable mode of measuring light-induced fluctuations in the intracellular calcium levels was also investigated with a view to observing the impact of the pharmacological agents on intracellular calcium concentration. This investigation has enhanced the understanding of the S. officinalis visual system by greatly adding to the present knowledge of the second messenger signalling cascade and by giving an insight into how this transfers into the animal's temporal resolving power. Some preliminary information regarding the membrane currents activated by light has also been presented. This has all been possible by the development of a versatile retinal slice preparation that has been proven to be accessible to extracellular recording and whole cell patch clamp recording combined with pharmacological manipulation.The Marine Biological Associatio