Synaptic mechanisms of adaptation and sensitization in the retina

Nature Neuroscience

Volumn 16, Issue 7, 2013, Pages 934-941

  Nikolaev, Anton ^a   Leung, Kin Mei ^a   Odermatt, Benjamin ^a   Lagnado, Leon ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; PICROTOXIN; TRICAINE;

ANIMAL EXPERIMENT; ARTICLE; CONTRAST; FACILITATION; FEEDBACK SYSTEM; GABAERGIC SYSTEM; IN VIVO STUDY; NERVE CELL; NERVE CELL PLASTICITY; NERVE ENDING; NERVE POTENTIAL; NONHUMAN; PHOTOSENSITIZATION; PHOTOSTIMULATION; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; SENSORY SYSTEM; SYNAPTIC TRANSMISSION; VISUAL ADAPTATION; VISUAL STIMULATION; ZEBRA FISH;

ADAPTATION, OCULAR; AMINOBENZOATES; ANESTHETICS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CENTRAL NERVOUS SYSTEM STIMULANTS; FEEDBACK, PHYSIOLOGICAL; LIGHT; NEURAL INHIBITION; NEURONS; PARVALBUMINS; PHOSPHOPYRUVATE HYDRATASE; PHOTIC STIMULATION; PICROTOXIN; PRESYNAPTIC TERMINALS; RETINA; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; VISUAL PATHWAYS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84879691838     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3408     Document Type: Article

References (50)

1. Wark, B., Lundstrom, B.N. & Fairhall, A. Sensory adaptation. Curr. Opin. Neurobiol. 17, 423-429 (2007).
2. Kohn, A. Visual adaptation: physiology, mechanisms, and functional benefits. J. Neurophysiol. 97, 3155-3164 (2007).
3. Rieke, F. & Rudd, M.E. The challenges natural images pose for visual adaptation. Neuron 64, 605-616 (2009).
4. Smirnakis, S.M., Berry, M.J., Warland, D.K., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69-73 (1997).
5. Wark, B., Fairhall, A. & Rieke, F. Timescales of inference in visual adaptation. Neuron 61, 750-761 (2009).
6. Laughlin, S.B. The role of sensory adaptation in the retina. J. Exp. Biol. 146, 39-62 (1989).
7. Demb, J.B. Functional circuitry of visual adaptation in the retina. J. Physiol. (Lond.) 586, 4377-4384 (2008).
8. Kastner, D.B. & Baccus, S.A. Coordinated dynamic encoding in the retina using opposing forms of plasticity. Nat. Neurosci. 14, 1317-1322 (2011).
9. Kim, K.J. & Rieke, F. Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J. Neurosci. 21, 287-299 (2001).
10. Baccus, S.A. & Meister, M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909-919 (2002).
11. Zaghloul, K.A., Boahen, K. & Demb, J.B. Contrast adaptation in subthreshold and spiking responses of mammalian Y-type retinal ganglion cells. J. Neurosci. 25, 860-868 (2005).
12. Manookin, M.B. & Demb, J.B. Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50, 453-464 (2006).
13. Beaudoin, D.L., Borghuis, B.G. & Demb, J.B. Cellular basis for contrast gain control over the receptive field center of mammalian retinal ganglion cells. J. Neurosci. 27, 2636-2645 (2007).
14. Baccus, S.A. Timing and computation in inner retinal circuitry. Annu. Rev. Physiol. 69, 271-290 (2007).
15. Gollisch, T. & Meister, M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65, 150-164 (2010).
16. Odermatt, B., Nikolaev, A. & Lagnado, L. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73, 758-773 (2012).
17. Dreosti, E. & Lagnado, L. Optical reporters of synaptic activity in neural circuits. Exp. Physiol. 96, 4-12 (2011).
18. Dreosti, E., Odermatt, B., Dorostkar, M.M. & Lagnado, L. A genetically encoded reporter of synaptic activity in vivo. Nat. Methods 6, 883-889 (2009).
19. Lagnado, L., Gomis, A. & Job, C. Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17, 957-967 (1996).
20. Ratliff, C.P., Borghuis, B.G., Kao, Y.H., Sterling, P. & Balasubramanian, V. Retina is structured to process an excess of darkness in natural scenes. Proc. Natl. Acad. Sci. USA 107, 17368-17373 (2010).
21. Hosoya, T., Baccus, S.A. & Meister, M. Dynamic predictive coding by the retina. Nature 436, 71-77 (2005).
22. DeVries, S.H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847-856 (2000).
23. Baden, T., Esposti, F., Nikolaev, A. & Lagnado, L. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 21, 1859-1869 (2011).
24. Dittman, J.S., Kreitzer, A.C. & Regehr, W.G. Interplay between facilitation, depression and residual calcium at three presynaptic terminals. J. Neurosci. 20, 1374-1385 (2000).
25. Gomis, A., Burrone, J. & Lagnado, L. Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J. Neurosci. 19, 6309-6317 (1999).
26. Burrone, J. & Lagnado, L. Synaptic depression and the kinetics of exocytosis in retinal bipolar cells. J. Neurosci. 20, 568-578 (2000).
27. Singer, J.H. & Diamond, J.S. Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J. Neurophysiol. 95, 3191-3198 (2006).
28. Ozuysal, Y. & Baccus, S.A. Linking the computational structure of variance adaptation to biophysical mechanisms. Neuron 73, 1002-1015 (2012).
29. Lukasiewicz, P.D., Maple, B.R. & Werblin, F.S. A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. J. Neurosci. 14, 1202-1212 (1994).
30. Jusuf, P.R. & Harris, W.A. Ptf1a is expressed transiently in all types of amacrine cells in the embryonic zebrafish retina. Neural Dev. 4, 34 (2009).
31. Nikolaou, N. et al. Parametric functional maps of visual inputs to the tectum. Neuron 76, 317-324 (2012).
32. Emran, F. et al. OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc. Natl. Acad. Sci. USA 104, 19126-19131 (2007).
33. Connaughton, V.P., Graham, D. & Nelson, R. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477, 371-385 (2004).
34. Wässle, H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5, 747-757 (2004).
35. Brown, S.P. & Masland, R.H. Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells. Nat. Neurosci. 4, 44-51 (2001).
36. Kim, K.J. & Rieke, F. Slow Na+ inactivation and variance adaptation in salamander retinal ganglion cells. J. Neurosci. 23, 1506-1516 (2003).
37. Jarsky, T. et al. A synaptic mechanism for retinal adaptation to luminance and contrast. J. Neurosci. 31, 11003-11015 (2011).
38. Sagdullaev, B.T., Eggers, E.D., Purgert, R. & Lukasiewicz, P.D. Nonlinear interactions between excitatory and inhibitory retinal synapses control visual output. J. Neurosci. 31, 15102-15112 (2011).
39. Heidelberger, R. & Matthews, G. Inhibition of calcium influx and calcium current by gamma-aminobutyric acid in single synaptic terminals. Proc. Natl. Acad. Sci. USA 88, 7135-7139 (1991).
40. Oesch, N.W. & Diamond, J.S. Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat. Neurosci. 14, 1555-1561 (2011).
41. Berglund, K., Midorikawa, M. & Tachibana, M. Increase in the pool size of releasable synaptic vesicles by the activation of protein kinase C in goldfish retinal bipolar cells. J. Neurosci. 22, 4776-4785 (2002).
42. Vickers, E., Kim, M.H., Vigh, J. & von Gersdorff, H. Paired-pulse plasticity in the strength and latency of light-evoked lateral inhibition to retinal bipolar cell terminals. J. Neurosci. 32, 11688-11699 (2012).
43. Dorostkar, M.M., Dreosti, E., Odermatt, B. & Lagnado, L. Computational processing of optical measurements of neuronal and synaptic activity in networks. J. Neurosci. Methods 188, 141-150 (2010).
44. Nusslein-Volhard, C. & Dahm, R. Zebrafish (Oxford University Press, Oxford, New York, 2002).
45. Ren, J.Q., McCarthy, W.R., Zhang, H., Adolph, A.R. & Li, L. Behavioral visual responses of wild-type and hypopigmented zebrafish. Vision Res. 42, 293-299 (2002).
46. Heidelberger, R., Zhou, Z.Y. & Matthews, G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J. Neurophysiol. 88, 2509-2517 (2002).
47. Hull, C. & von Gersdorff, H. Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44, 469-482 (2004).
48. Neves, G. & Lagnado, L. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. (Lond.) 515, 181-202 (1999).
49. Neves, G. & Lagnado, L. Visual processing: the devil is in the details. Curr. Biol. 10, R896-R898 (2000).
50. Bai, Q., Wei, X. & Burton, E.A. Expression of a 12-kb promoter element derived from the zebrafish enolase-2 gene in the zebrafish visual system. Neurosci. Lett. 449, 252-257 (2009).