Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: I Dynamics

Because of the limited processing capacity of eyes, retinal networks must adapt constantly to best present the ever changing visual world to the brain. However, we still know little about how adaptation in retinal networks shapes neural encoding of changing information. To study this question, we recorded voltage responses from photoreceptors (R1–R6) and their output neurons (LMCs) in the Drosophila eye to repeated patterns of contrast values, collected from natural scenes. By analyzing the continuous photoreceptor-to-LMC transformations of these graded-potential neurons, we show that the efficiency of coding is dynamically improved by adaptation. In particular, adaptation enhances both the frequency and amplitude distribution of LMC output by improving sensitivity to under-represented signals within seconds. Moreover, the signal-to-noise ratio of LMC output increases in the same time scale. We suggest that these coding properties can be used to study network adaptation using the genetic tools in Drosophila, as shown in a companion paper (Part II).

[1]  Haruo Kasai,et al.  Protein Synthesis and Neurotrophin-Dependent Structural Plasticity of Single Dendritic Spines , 2008, Science.

[2]  Michael J. Berry,et al.  Selectivity for multiple stimulus features in retinal ganglion cells. , 2006, Journal of neurophysiology.

[3]  Robert A. Hummel,et al.  Image Enhancement by Histogram transformation , 1975 .

[4]  Jaeseob Kim,et al.  Histamine and Its Receptors Modulate Temperature-Preference Behaviors in Drosophila , 2006, The Journal of Neuroscience.

[5]  S B Laughlin,et al.  Voltage‐activated potassium channels in blowfly photoreceptors and their role in light adaptation. , 1991, The Journal of physiology.

[6]  H. P. Snippe,et al.  Phototransduction in primate cones and blowfly photoreceptors: different mechanisms, different algorithms, similar response , 2005, Journal of Comparative Physiology A.

[7]  Robert J. Moorhead,et al.  Visualization of fluid flows in virtual environments , 2004, J. Vis..

[8]  S. N. Fry,et al.  The aerodynamics of hovering flight in Drosophila , 2005, Journal of Experimental Biology.

[9]  Ralph Linsker,et al.  An Application of the Principle of Maximum Information Preservation to Linear Systems , 1988, NIPS.

[10]  Matti Järvilehto,et al.  Localized intracellular potentials from pre- and postsynaptic components in the external plexiform layer of an insect retina , 1971, Zeitschrift für vergleichende Physiologie.

[11]  Christof Koch,et al.  How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate , 1999, Nature Neuroscience.

[12]  Joseph J. Atick,et al.  Towards a Theory of Early Visual Processing , 1990, Neural Computation.

[13]  S. Arom,et al.  African polyphony and polyrhythm: Description and analysis , 1991 .

[14]  B. Burton Long-term light adaptation in photoreceptors of the housefly, Musca domestica , 2002, Journal of Comparative Physiology A.

[15]  Reinhard Wolf,et al.  Visual Pattern Recognition in Drosophila Is Invariant for Retinal Position , 2004, Science.

[16]  X. Breakefield Neurogenetics : genetic approaches to the nervous system , 1979 .

[17]  N. Strausfeld,et al.  Dissection of the Peripheral Motion Channel in the Visual System of Drosophila melanogaster , 2007, Neuron.

[18]  J. H. van Hateren,et al.  Real and optimal neural images in early vision , 1992, Nature.

[19]  Roger C. Hardie,et al.  Visual transduction in Drosophila , 2001, Nature.

[20]  I. Meinertzhagen,et al.  Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. , 2001, Progress in brain research.

[21]  Roger C. Hardie,et al.  Feedback Network Controls Photoreceptor Output at the Layer of First Visual Synapses in Drosophila , 2006, The Journal of general physiology.

[22]  Mikko Vähäsöyrinki,et al.  Robustness of Neural Coding in Drosophila Photoreceptors in the Absence of Slow Delayed Rectifier K+ Channels , 2006, The Journal of Neuroscience.

[23]  Adrienne L. Fairhall,et al.  Efficiency and ambiguity in an adaptive neural code , 2001, Nature.

[24]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[25]  Michael J. Berry,et al.  Sophisticated temporal pattern recognition in retinal ganglion cells. , 2008, Journal of neurophysiology.

[26]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[27]  R. Hardie,et al.  A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse , 1989, Nature.

[28]  Joseph J Atick,et al.  Could information theory provide an ecological theory of sensory processing? , 2011, Network.

[29]  A. S. French,et al.  Information processing by graded-potential transmission through tonically active synapses , 1996, Trends in Neurosciences.

[30]  Ian A. Meinertzhagen,et al.  Glutamate, GABA and Acetylcholine Signaling Components in the Lamina of the Drosophila Visual System , 2008, PloS one.

[31]  R. Hardie,et al.  Three classes of potassium channels in large monopolar cells of the blowfly Calliphora vicina , 1990, Journal of Comparative Physiology A.

[32]  S. N. Fry,et al.  The Aerodynamics of Free-Flight Maneuvers in Drosophila , 2003, Science.

[33]  J. Miller,et al.  Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system. , 1997, Journal of neurophysiology.

[34]  Roger C. Hardie,et al.  Distinct Roles for Two Histamine Receptors (hclA and hclB) at the Drosophila Photoreceptor Synapse , 2008, The Journal of Neuroscience.

[35]  V. Hateren,et al.  Processing of natural time series of intensities by the visual system of the blowfly , 1997, Vision Research.

[36]  Mikko Juusola,et al.  Impact of rearing conditions and short-term light exposure on signaling performance in Drosophila photoreceptors. , 2004, Journal of neurophysiology.

[37]  J. P. Lindemann,et al.  Function of a Fly Motion-Sensitive Neuron Matches Eye Movements during Free Flight , 2005, PLoS biology.

[38]  Shin-ya Takemura,et al.  Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla , 2008, The Journal of comparative neurology.

[39]  J. Armitage,et al.  Absolute Contrast Enhancement , 1965 .

[40]  J. V. van Hateren,et al.  Real and optimal neural images in early vision , 1992, Nature.

[41]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

[42]  G. Buchsbaum,et al.  Trichromacy, opponent colours coding and optimum colour information transmission in the retina , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[43]  Kenneth D. Miller,et al.  Adaptive filtering enhances information transmission in visual cortex , 2006, Nature.

[44]  Gonzalo G. de Polavieja,et al.  The Rate of Information Transfer of Naturalistic Stimulation by Graded Potentials , 2003, The Journal of general physiology.

[45]  A. Fairhall,et al.  Sensory adaptation , 2007, Current Opinion in Neurobiology.

[46]  R. O. Uusitalo,et al.  Tonic transmitter release in a graded potential synapse. , 1995, Journal of neurophysiology.

[47]  Martin Heisenberg,et al.  The rôle of retinula cell types in visual behavior ofDrosophila melanogaster , 2004, Journal of comparative physiology.

[48]  S B Laughlin,et al.  Synaptic limitations to contrast coding in the retina of the blowfly Calliphora , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[49]  T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[50]  Gonzalo G de Polavieja Errors drive the evolution of biological signalling to costly codes. , 2002, Journal of theoretical biology.

[51]  A S French,et al.  Nonlinear models of the first synapse in the light-adapted fly retina. , 1995, Journal of neurophysiology.

[52]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[53]  David C. O'Carroll,et al.  Implementation of an elaborated neuromorphic model of a biological photoreceptor , 2008, Biological Cybernetics.

[54]  M. Heisenberg,et al.  Vision in Drosophila: Genetics of Microbehavior , 2011 .

[55]  S. Shaw Early visual processing in insects. , 1984, The Journal of experimental biology.

[56]  R. O. Uusitalo,et al.  Transfer of graded potentials at the photoreceptor-interneuron synapse , 1995, The Journal of general physiology.

[57]  D. Pinkel,et al.  Supporting Online Material Materials and Methods Figs. S1 and S2 Tables S1 and S2 References Combined Analog and Action Potential Coding in Hippocampal Mossy Fibers , 2022 .

[58]  Eng-Leng Mah,et al.  Photoreceptor processing improves salience facilitating small target detection in cluttered scenes. , 2008, Journal of vision.

[59]  D J Field,et al.  Relations between the statistics of natural images and the response properties of cortical cells. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[60]  F. Werblin,et al.  Inhibitory feedback shapes bipolar cell responses in the rabbit retina. , 2007, Journal of neurophysiology.

[61]  Nicholas J. Strausfeld,et al.  The compound eye of the fly (Musca domestica): connections between the cartridges of the lamina ganglionaris , 1970, Zeitschrift für vergleichende Physiologie.

[62]  W. J. Heitler,et al.  The effects of temperature on the threshold of identified neurons in the locust , 2004, Journal of comparative physiology.

[63]  Adam Kepecs,et al.  Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making , 2006, Nature Reviews Neuroscience.

[64]  J. H. Hateren,et al.  Information theoretical evaluation of parametric models of gain control in blowfly photoreceptor cells , 2001, Vision Research.

[65]  I. Meinertzhagen,et al.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster , 1991, The Journal of comparative neurology.

[66]  K. Kirschfeld,et al.  Die projektion der optischen umwelt auf das raster der rhabdomere im komplexauge von Musca , 2004, Experimental Brain Research.

[67]  A S French,et al.  Visual acuity for moving objects in first- and second-order neurons of the fly compound eye. , 1997, Journal of neurophysiology.

[68]  Roger C. Hardie,et al.  Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly , 1978, Journal of comparative physiology.

[69]  F. Attneave Some informational aspects of visual perception. , 1954, Psychological review.

[70]  H. Sompolinsky,et al.  Adaptation without parameter change: Dynamic gain control in motion detection , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[71]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[72]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[73]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors: II. Rising Temperature Increases the Bandwidth of Reliable Signaling , 2001 .

[74]  Michael J. Berry,et al.  Redundancy in the Population Code of the Retina , 2005, Neuron.

[75]  C. Goodman,et al.  Synapse-specific control of synaptic efficacy at the terminals of a single neuron , 1998, Nature.

[76]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors: I. Response Dynamics and Signaling Efficiency at 25°C , 2001 .

[77]  M. Meister,et al.  Fast and Slow Contrast Adaptation in Retinal Circuitry , 2002, Neuron.

[78]  Structural daily rhythms in GFP-labelled neurons in the visual system of Drosophila melanogaster. , 2005, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[79]  Eric Warrant,et al.  Vision in the dimmest habitats on Earth , 2004, Journal of Comparative Physiology A.

[80]  R. Wolf,et al.  On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster , 2004, Journal of comparative physiology.

[81]  T. Collett,et al.  Chasing behaviour of houseflies (Fannia canicularis) , 1974, Journal of comparative physiology.

[82]  D. McCormick,et al.  Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential , 2006, Nature.

[83]  Michael J. Berry,et al.  Role of eye movements in the retinal code for a size discrimination task. , 2007, Journal of neurophysiology.

[84]  R C Reid,et al.  Efficient Coding of Natural Scenes in the Lateral Geniculate Nucleus: Experimental Test of a Computational Theory , 1996, The Journal of Neuroscience.

[85]  Andreas S. Thum,et al.  The Neural Substrate of Spectral Preference in Drosophila , 2008, Neuron.

[86]  R. Hengstenberg,et al.  Estimation of self-motion by optic flow processing in single visual interneurons , 1996, Nature.

[87]  Burton-Bradley Bg Long-term light adaptation in photoreceptors of the housefly, Musca domestica. , 2002 .

[88]  Gonzalo G de Polavieja Reliable biological communication with realistic constraints. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[89]  A. Fairhall,et al.  Fractional differentiation by neocortical pyramidal neurons , 2008, Nature Neuroscience.

[90]  M. Juusola Linear and non-linear contrast coding in light-adapted blowfly photoreceptors , 1993, Journal of Comparative Physiology A.

[91]  M. Heisenberg,et al.  Vision in Drosophila , 1984 .

[92]  Karl Geokg Götz,et al.  Optomotorische Untersuchung des visuellen systems einiger Augenmutanten der Fruchtfliege Drosophila , 1964, Kybernetik.

[93]  Mikko Juusola,et al.  Coding with spike shapes and graded potentials in cortical networks. , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[94]  Mikko Juusola,et al.  Visual Coding in Locust Photoreceptors , 2008, PloS one.

[95]  Mikko Juusola,et al.  Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons , 2005, The Journal of Neuroscience.

[96]  Gonzalo G. de Polavieja,et al.  Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: II Mechanisms , 2009, PloS one.

[97]  M Järvilehto,et al.  Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors , 1994, The Journal of general physiology.

[98]  Irina Sinakevitch,et al.  Chemical neuroanatomy of the fly's movement detection pathway , 2004, The Journal of comparative neurology.

[99]  R. O. Uusitalo,et al.  Graded responses and spiking properties of identified first-order visual interneurons of the fly compound eye. , 1995, Journal of neurophysiology.

[100]  J. H. Hateren,et al.  Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation , 1992, Journal of Comparative Physiology A.

[101]  A. Straw,et al.  Contrast sensitivity of insect motion detectors to natural images. , 2008, Journal of vision.

[102]  S. Benzer,et al.  Behavioral genetics of thermosensation and hygrosensation in Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[103]  R. Hardie,et al.  The Target of Drosophila Photoreceptor Synaptic Transmission Is a Histamine-gated Chloride Channel Encoded byort (hclA)* , 2002, The Journal of Biological Chemistry.

[104]  S. Laughlin,et al.  The rate of information transfer at graded-potential synapses , 1996, Nature.

[105]  R. Wolf,et al.  On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster , 1979, Journal of comparative physiology.

[106]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[107]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[108]  J. Atick,et al.  STATISTICS OF NATURAL TIME-VARYING IMAGES , 1995 .

[109]  Simon B Laughlin,et al.  Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica , 2003, Journal of Experimental Biology.

[110]  S. Laughlin A Simple Coding Procedure Enhances a Neuron's Information Capacity , 1981, Zeitschrift fur Naturforschung. Section C, Biosciences.

[111]  J. V. van Hateren A model of spatiotemporal signal processing by primate cones and horizontal cells. , 2007, Journal of vision.

[112]  D. Stavenga Angular and spectral sensitivity of fly photoreceptors. II. Dependence on facet lens F-number and rhabdomere type in Drosophila , 2003, Journal of Comparative Physiology A.