Effects of dopamine on response properties of ON-OFF RGCs in encoding stimulus durations

Single retinal ganglion cell's (RGCs) response properties, such as spike count and response latency, are known to encode some features of visual stimuli. On the other hand, neuronal response can be modulated by dopamine (DA), an important endogenous neuromodulator in the retina. In the present study, we investigated the effects of DA on the spike count and the response latency of bullfrog ON-OFF RGCs during exposure to different stimulus durations. We found that neuronal spike count and response latency were both changed with stimulus durations, and exogenous DA (10 μM) obviously attenuated the stimulus-duration-dependent response latency change. Information analysis showed that the information about light ON duration was mainly carried by the OFF response and vice versa, and the stimulation information was carried by both spike count and response latency. However, during DA application, the information carried by the response latency was greatly decreased, which suggests that dopaminergic pathway is involved in modulating the role of response latency in encoding the information about stimulus durations.

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

[2]  P. Witkovsky,et al.  Glutamate release by the intact light-responsive photoreceptor layer of the Xenopus retina , 1996, Journal of Neuroscience Methods.

[3]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

[4]  J Clark Frank,et al.  Information Processing , 1970 .

[5]  J D Pitts,et al.  The Gap Junction , 1986, Journal of Cell Science.

[6]  P. Liang,et al.  Influence of GABAergic inhibition on concerted activity between the ganglion cells , 2010, Neuroreport.

[7]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[8]  Xiong-Li Yang.  Characterization of receptors for glutamate and GABA in retinal neurons , 2004, Progress in Neurobiology.

[9]  M. Tachibana,et al.  Synchronized retinal oscillations encode essential information for escape behavior in frogs , 2005, Nature Neuroscience.

[10]  E. A. Schwartz,et al.  Responses of bipolar cells in the retina of the turtle , 1974, The Journal of physiology.

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

[12]  Si Wu,et al.  Shifted encoding strategy in retinal luminance adaptation: from firing rate to neural correlation. , 2013, Journal of neurophysiology.

[13]  P. Detwiler,et al.  Different Mechanisms Generate Maintained Activity in ON and OFF Retinal Ganglion Cells , 2007, The Journal of Neuroscience.

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

[15]  Paul Witkovsky,et al.  Dopamine and retinal function , 2004, Documenta Ophthalmologica.

[16]  Daeyeol Lee,et al.  Coding and transmission of information by neural ensembles , 2004, Trends in Neurosciences.

[17]  J. Dowling,et al.  Effects of Dopamine Depletion on Visual Sensitivity of Zebrafish , 2000, The Journal of Neuroscience.

[18]  F. Mechler,et al.  Temporal coding of contrast in primary visual cortex: when, what, and why. , 2001, Journal of neurophysiology.

[19]  Guo-yong Wang,et al.  Dopamine modulates the off pathway in light‐adapted mouse retina , 2012, Journal of neuroscience research.

[20]  Jonathan D Victor,et al.  Spike train metrics , 2005, Current Opinion in Neurobiology.

[21]  Yi Zhou,et al.  Spike sorting based on automatic template reconstruction with a partial solution to the overlapping problem , 2004, Journal of Neuroscience Methods.

[22]  S.M. Harris,et al.  Information Processing , 1977, Nature.

[23]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[24]  W. Pitts,et al.  Anatomy and Physiology of Vision in the Frog (Rana pipiens) , 1960, The Journal of general physiology.

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

[26]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[27]  E. Popova,et al.  Effects of dopamine D1 receptor blockade on the intensity-response function of ERG b- and d-waves under different conditions of light adaptation , 2011, Vision Research.

[28]  P. Liang,et al.  Stimulus discrimination via responses of retinal ganglion cells and dopamine-dependent modulation , 2013, Neuroscience Bulletin.

[29]  G D Field,et al.  Information processing in the primate retina: circuitry and coding. , 2007, Annual review of neuroscience.

[30]  S. DeVries.  Correlated firing in rabbit retinal ganglion cells. , 1999, Journal of neurophysiology.

[31]  B. Völgyi,et al.  The diverse functional roles and regulation of neuronal gap junctions in the retina , 2009, Nature Reviews Neuroscience.

[32]  Si Wu,et al.  Response dynamics of bullfrog ON-OFF RGCs to different stimulus durations , 2014, Journal of Computational Neuroscience.

[33]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

[34]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[35]  R. Masland.  The Neuronal Organization of the Retina , 2012, Neuron.

[36]  Rasmus S Petersen,et al.  Comparison of latency and rate coding for the direction of whisker deflection in the subcortical somatosensory pathway. , 2012, Journal of neurophysiology.

[37]  C. Nicholson,et al.  Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Palmiter,et al.  Retinal Dopamine Mediates Multiple Dimensions of Light-Adapted Vision , 2012, The Journal of Neuroscience.

[39]  Stefano Panzeri,et al.  Analytical estimates of limited sampling biases in different information measures. , 1996, Network.

[40]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[41]  N. Wioland,et al.  Effects of some amino acids (GABA, glycine, taurine) and of their antagonists (picrotoxin, strychnine) on spatial and temporal features of frog retinal ganglion cell responses , 1980, Pflügers Archiv.

[42]  Eric D Young,et al.  First-spike latency information in single neurons increases when referenced to population onset , 2007, Proceedings of the National Academy of Sciences.

[43]  P. Liang,et al.  Adaptation-Dependent Synchronous Activity Contributes to Receptive Field Size Change of Bullfrog Retinal Ganglion Cell , 2012, PloS one.

[44]  F. Werblin,et al.  Dopamine enhances a glutamate-gated ionic current in OFF bipolar cells of the tiger salamander retina , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  M. Greschner,et al.  Contribution of individual retinal ganglion cell responses to velocity and acceleration encoding. , 2007, Journal of neurophysiology.

[46]  Yin Shen,et al.  Regulation of ON bipolar cell activity , 2008, Progress in Retinal and Eye Research.

[47]  J. B. Demb,et al.  Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight , 2008, The Journal of Neuroscience.

[48]  M. Greschner,et al.  Complex spike-event pattern of transient ON-OFF retinal ganglion cells. , 2006, Journal of neurophysiology.

[49]  Jonathan D. Victor,et al.  Metric-space analysis of spike trains: theory, algorithms and application , 1998, q-bio/0309031.

[50]  Hao Li,et al.  Gap junction permeability modulated by dopamine exerts effects on spatial and temporal correlation of retinal ganglion cells’ firing activities , 2013, Journal of Computational Neuroscience.

[51]  Nicholas W. Oesch,et al.  Illuminating synapses and circuitry in the retina , 2011, Current Opinion in Neurobiology.

[52]  F. Amthor,et al.  The response dynamics of rabbit retinal ganglion cells to simulated blur , 2010, Visual Neuroscience.

[53]  Paul Witkovsky,et al.  Chapter 10 Functional roles of dopamine in the vertebrate retina , 1991 .

[54]  Norberto M Grzywacz,et al.  Separability of stimulus parameter encoding by on-off directionally selective rabbit retinal ganglion cells. , 2011, Journal of neurophysiology.