Frontiers in Computational Neuroscience Computational Neuroscience

An animal's ability to rapidly adjust to new conditions is essential to its survival. The nervous system, then, must be built with the flexibility to adjust, or shift, its processing capabilities on the fly. To understand how this flexibility comes about, we tracked a well-known behavioral shift, a visual integration shift, down to its underlying circuitry, and found that it is produced by a novel mechanism – a change in gap junction coupling that can turn a cell class on and off. The results showed that the turning on and off of a cell class shifted the circuit's behavior from one state to another, and, likewise, the animal's behavior. The widespread presence of similar gap junction-coupled networks in the brain suggests that this mechanism may underlie other behavioral shifts as well.

[1]  D. Baylor,et al.  Mosaic arrangement of ganglion cell receptive fields in rabbit retina. , 1997, Journal of neurophysiology.

[2]  F. Rieke,et al.  Bandpass Filtering at the Rod to Second-Order Cell Synapse in Salamander (Ambystoma tigrinum) Retina , 2003, The Journal of Neuroscience.

[3]  Scott J. Daly,et al.  Temporal information processing in cones: Effects of light adaptation on temporal summation and modulation , 1985, Vision Research.

[4]  M. Antoch,et al.  The Murine Cone Photoreceptor A Single Cone Type Expresses Both S and M Opsins with Retinal Spatial Patterning , 2000, Neuron.

[5]  H. Barlow The efficiency of detecting changes of density in random dot patterns , 1978, Vision Research.

[6]  J B Troy,et al.  Characteristics of the Sony Multiscan 17se Trinitron color graphic display. , 1997, Spatial vision.

[7]  S. Nirenberg,et al.  Selective Ablation of a Class of Amacrine Cells Alters Spatial Processing in the Retina , 2004, The Journal of Neuroscience.

[8]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[9]  K. Naka,et al.  The generation and spread of S‐potentials in fish (Cyprinidae) , 1967, The Journal of physiology.

[10]  T. Hughes,et al.  Signals and systems , 2006, Genome Biology.

[11]  M. McCall,et al.  Stimulus size and intensity alter fundamental receptive-field properties of mouse retinal ganglion cells in vivo , 2005, Visual Neuroscience.

[12]  Mark Pottek,et al.  Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine , 2000, Brain Research Reviews.

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

[14]  J. Dowling The Retina: An Approachable Part of the Brain , 1988 .

[15]  C. Koch,et al.  Methods in Neuronal Modeling: From Ions to Networks , 1998 .

[16]  Timm Schubert,et al.  Functional expression of connexin57 in horizontal cells of the mouse retina , 2004, The European journal of neuroscience.

[17]  Helga Kolb,et al.  Rod and Cone Pathways in the Inner Plexiform Layer of Cat Retina , 1974, Science.

[18]  T E Cohn,et al.  Noise and its effects on photoreceptor temporal contrast sensitivity at low light levels. , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[19]  M. Carandini,et al.  The Statistical Computation Underlying Contrast Gain Control , 2006, The Journal of Neuroscience.

[20]  S. Bloomfield,et al.  Rod Vision: Pathways and Processing in the Mammalian Retina , 2001, Progress in Retinal and Eye Research.

[21]  Wilson S. Geisler,et al.  Ideal observer theory in psychophysics and physiology , 1989 .

[22]  Fred Rieke,et al.  Signals and noise in an inhibitory interneuron diverge to control activity in nearby retinal ganglion cells , 2008, Nature Neuroscience.

[23]  R M Douglas,et al.  Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system , 2005, Visual Neuroscience.

[24]  Norbert Babai,et al.  Horizontal cell feedback regulates calcium currents and intracellular calcium levels in rod photoreceptors of salamander and mouse retina , 2009, The Journal of physiology.

[25]  J. A. Hirsch Synaptic physiology and receptive field structure in the early visual pathway of the cat. , 2003, Cerebral cortex.

[26]  G. I. Hatton,et al.  Histamine H1-receptor modulation of inter-neuronal coupling among vasopressinergic neurons depends on nitric oxide synthase activation , 2002, Brain Research.

[27]  Chethan Pandarinath,et al.  Ganglion Cell Adaptability: Does the Coupling of Horizontal Cells Play a Role? , 2008, PloS one.

[28]  Edward N. Pugh,et al.  Physiological Features of the S- and M-cone Photoreceptors of Wild-type Mice from Single-cell Recordings , 2006, The Journal of general physiology.

[29]  D. Dacey,et al.  Synergistic center-surround receptive field model of monkey H1 horizontal cells. , 2005, Journal of vision.

[30]  T. Lamb,et al.  Spatial properties of horizontal cell responses in the turtle retina. , 1976, The Journal of physiology.

[31]  Erika D Eggers,et al.  Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina , 2007, The Journal of physiology.

[32]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[33]  H. Wässle,et al.  Synaptic Currents Generating the Inhibitory Surround of Ganglion Cells in the Mammalian Retina , 2001, The Journal of Neuroscience.

[34]  A. Fairhall,et al.  Timescales of Inference in Visual Adaptation , 2009, Neuron.

[35]  J. B. Demb,et al.  Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities , 2003, The Journal of Neuroscience.

[36]  John P. Walsh,et al.  Dye-Coupling in the Neostriatum of the Rat , 1991 .

[37]  E. Kaplan,et al.  Dynamics of primate P retinal ganglion cells: responses to chromatic and achromatic stimuli , 1999, The Journal of physiology.

[38]  Timm Schubert,et al.  Horizontal cell receptive fields are reduced in connexin57‐deficient mice , 2006, The European journal of neuroscience.

[39]  C S Peskin,et al.  How to See in the Dark: Photon Noise in Vision and Nuclear Medicine a , 1984, Annals of the New York Academy of Sciences.

[40]  J. Dowling,et al.  Horizontal cell gap junctions: single-channel conductance and modulation by dopamine. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Alice Z Chuang,et al.  Photoreceptor Coupling Is Controlled by Connexin 35 Phosphorylation in Zebrafish Retina , 2009, The Journal of Neuroscience.

[42]  S. M. Wu,et al.  Feedforward lateral inhibition in retinal bipolar cells: input-output relation of the horizontal cell-depolarizing bipolar cell synapse. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  P. Latham,et al.  Synergy, Redundancy, and Independence in Population Codes, Revisited , 2005, The Journal of Neuroscience.

[44]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[45]  T E Cohn,et al.  A new hypothesis to explain why the increment threshold exceeds the decrement threshold. , 1974, Vision research.

[46]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[47]  D. Baylor,et al.  Visual transduction in cones of the monkey Macaca fascicularis. , 1990, The Journal of physiology.

[48]  E. Chichilnisky,et al.  Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina , 2002, The Journal of Neuroscience.

[49]  R. G. Smith,et al.  Simulation of an anatomically defined local circuit: The cone-horizontal cell network in cat retina , 1995, Visual Neuroscience.

[50]  Yumiko Umino,et al.  Speed, Spatial, and Temporal Tuning of Rod and Cone Vision in Mouse , 2008, The Journal of Neuroscience.

[51]  X L Yang,et al.  Effects of background illumination on the horizontal cell responses in the tiger salamander retina , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  D. Baylor,et al.  Receptive fields of cones in the retina of the turtle , 1971, The Journal of physiology.

[53]  B. Völgyi,et al.  Convergence and Segregation of the Multiple Rod Pathways in Mammalian Retina , 2004, The Journal of Neuroscience.

[54]  Vijay Balasubramanian,et al.  Receptive fields and functional architecture in the retina , 2009, The Journal of physiology.

[55]  J. Dowling,et al.  Intracellular recordings from gecko photoreceptors during light and dark adaptation , 1975, The Journal of general physiology.

[56]  J. Victor The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[57]  Partha P. Mitra,et al.  Observed Brain Dynamics , 2007 .

[58]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[59]  W R Taylor,et al.  TTX attenuates surround inhibition in rabbit retinal ganglion cells , 1999, Visual Neuroscience.

[60]  S. Bloomfield,et al.  Light-induced modulation of coupling between AII amacrine cells in the rabbit retina , 1997, Visual Neuroscience.

[61]  G. Maccaferri,et al.  Noradrenergic Modulation of Electrical Coupling in GABAergic Networks of the Hippocampus , 2008, The Journal of Neuroscience.

[62]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[63]  S. M. Wu,et al.  Modulation of rod-cone coupling by light. , 1989, Science.

[64]  K. Yau,et al.  Light Adaptation in Retinal Rods of the Rabbit and Two Other Nonprimate Mammals Nakatani Et Al. Light Adaptation M Rabbit and Other Mammalian Rods Experiments on Cattle and Rat , 1991 .

[65]  F. Lui,et al.  The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. , 2006, Progress in brain research.

[66]  Mark P. Mattson,et al.  Horizontal cell electrical coupling in the giant danio: synaptic modulation by dopamine and synaptic maintenance by calcium , 1996, Brain Research.

[67]  J. L. Schnapf,et al.  Noise and light adaptation in rods of the macaque monkey , 2000, Visual Neuroscience.

[68]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[69]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[70]  J. McReynolds,et al.  The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. , 1991, The Journal of physiology.

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

[72]  M. Bennett,et al.  Electrical Coupling and Neuronal Synchronization in the Mammalian Brain , 2004, Neuron.

[73]  M. Abramowitz,et al.  Handbook of Mathematical Functions With Formulas, Graphs and Mathematical Tables (National Bureau of Standards Applied Mathematics Series No. 55) , 1965 .

[74]  D. H. Kelly Visual response to time-dependent stimuli. I. Amplitude sensitivity measurements. , 1961, Journal of the Optical Society of America.

[75]  K. Yau,et al.  Light adaptation in cat retinal rods. , 1989, Science.

[76]  M. A. Bouman,et al.  Spatiotemporal modulation transfer in the human eye. , 1967, Journal of the Optical Society of America.

[77]  Satoru Kato,et al.  Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina , 1983, Nature.

[78]  R. Douglas,et al.  Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. , 2004, Investigative ophthalmology & visual science.

[79]  J. B. Demb,et al.  Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina , 2001, The Journal of Neuroscience.

[80]  P. Latham,et al.  Retinal ganglion cells act largely as independent encoders , 2001, Nature.

[81]  I. Ohzawa,et al.  Contrast gain control in the cat visual cortex , 1982, Nature.

[82]  Timm Schubert,et al.  Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina , 2008, The Journal of Neuroscience.

[83]  Maarten Kamermans,et al.  Retinal horizontal cell‐specific promoter activity and protein expression of zebrafish connexin 52.6 and connexin 55.5 , 2007, The Journal of comparative neurology.

[84]  J. Walsh,et al.  Dye‐Coupling in the neostriatum of the rat: I. Modulation by dopamine‐depleting lesions , 1989, Synapse.

[85]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[86]  R. Shapley,et al.  Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells , 1990, Visual Neuroscience.

[87]  A. Grace,et al.  Dopamine and cyclic-AMP regulated phosphoprotein-32–dependent modulation of prefrontal cortical input and intercellular coupling in mouse accumbens spiny and aspiny neurons , 2008, Neuroscience.

[88]  P. E. Hallett,et al.  A schematic eye for the mouse, and comparisons with the rat , 1985, Vision Research.

[89]  E. Chichilnisky,et al.  Adaptation to Temporal Contrast in Primate and Salamander Retina , 2001, The Journal of Neuroscience.

[90]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[91]  D. Dacey,et al.  The Classical Receptive Field Surround of Primate Parasol Ganglion Cells Is Mediated Primarily by a Non-GABAergic Pathway , 2004, The Journal of Neuroscience.

[92]  Kerry J. Kim,et al.  Temporal Contrast Adaptation in the Input and Output Signals of Salamander Retinal Ganglion Cells , 2001, The Journal of Neuroscience.

[93]  Yu Wang,et al.  A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[94]  Milton Abramowitz,et al.  Handbook of Mathematical Functions with Formulas, Graphs, and Mathematical Tables , 1964 .

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

[96]  Fred Rieke,et al.  Network Variability Limits Stimulus-Evoked Spike Timing Precision in Retinal Ganglion Cells , 2006, Neuron.

[97]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[98]  John H. R. Maunsell,et al.  Feature-based attention in visual cortex , 2006, Trends in Neurosciences.

[99]  Joel Pokorny,et al.  Responses of macaque ganglion cells and human observers to compound periodic waveforms , 1993, Vision Research.

[100]  F S Werblin,et al.  Three Levels of Lateral Inhibition: A Space–Time Study of the Retina of the Tiger Salamander , 2000, The Journal of Neuroscience.

[101]  George Spindler,et al.  The Significance of Differences. , 1979 .

[102]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[103]  Terrence J. Sejnowski,et al.  Synaptic currents, neuromodulation, and kinetic models , 1998 .

[104]  E. Strettoi,et al.  Synaptic connections of the narrow‐field, bistratified rod amacrine cell (AII) in the rabbit retina , 1992, The Journal of comparative neurology.

[105]  C. Ribelayga,et al.  The Circadian Clock in the Retina Controls Rod-Cone Coupling , 2008, Neuron.

[106]  E. Buhl,et al.  Retinal ganglion cells projecting to the accessory optic system in the rat , 1987, The Journal of comparative neurology.

[107]  S. M. Wu,et al.  Response sensitivity and voltage gain of the rod- and cone-bipolar cell synapses in dark-adapted tiger salamander retina. , 1997, Journal of neurophysiology.

[108]  L. Peichl,et al.  Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig , 1994, Visual Neuroscience.

[109]  K. Yau,et al.  Rod Sensitivity of Neonatal Mouse and Rat , 2005, The Journal of general physiology.

[110]  M Kamermans,et al.  Hemichannel-Mediated Inhibition in the Outer Retina , 2001, Science.

[111]  S. Hestrin,et al.  Electrical synapses between Gaba-Releasing interneurons , 2001, Nature Reviews Neuroscience.

[112]  S. Bloomfield,et al.  Dark‐ and light‐induced changes in coupling between horizontal cells in mammalian retina , 1999, The Journal of comparative neurology.

[113]  Ji-Jie Pang,et al.  Light-Evoked Excitatory and Inhibitory Synaptic Inputs to ON and OFF α Ganglion Cells in the Mouse Retina , 2003, The Journal of Neuroscience.

[114]  P. Cook,et al.  Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells , 1998, Nature Neuroscience.

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

[116]  Christof Koch,et al.  A simple algorithm for solving the cable equation in dendritic trees of arbitrary geometry , 1985, Journal of Neuroscience Methods.

[117]  Gerrit Hilgen,et al.  Connexin57 is expressed in dendro‐dendritic and axo‐axonal gap junctions of mouse horizontal cells and its distribution is modulated by light , 2009, The Journal of comparative neurology.