Subthreshold membrane conductances enhance directional selectivity in vertebrate sensory neurons

Journal of Neurophysiology

Volumn 104, Issue 1, 2010, Pages 449-462

  Chacron, Maurice J ^a   Fortune, Eric S ^b,c  

^a MCGILL UNIVERSITY   (Canada)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MIBEFRADIL; NICKEL CHLORIDE; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; FISH; IN VIVO STUDY; INTRACELLULAR RECORDING; MATHEMATICAL MODEL; MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR INTEGRATION; SENSORY NERVE CELL;

ALGORITHMS; ANIMALS; CALCIUM CHANNEL BLOCKERS; CHLORIDE CHANNELS; ELECTRIC FISH; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; ION CHANNELS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; MODELS, STATISTICAL; MOTION PERCEPTION; MOVEMENT; NEURAL CONDUCTION; NEURAL PATHWAYS; NONLINEAR DYNAMICS; ORIENTATION; SENSORY RECEPTOR CELLS; SODIUM CHANNEL BLOCKERS;

EID: 77954445314     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01113.2009     Document Type: Article

References (56)

1. Adelson EH, Bergen JR. Spatiotemporal energy models for the perception of motion. J Opt Soc Am A Opt Image Sci 2: 284-299, 1985.
2. 2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci 18: 8740-8750, 1998.
3. Bastian J. Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J Comp Physiol [A] 144: 481-494, 1981.
4. Bastian J, Chacron MJ, Maler L. Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22: 4577-4590, 2002. (Pubitemid 37465674)
5. Berman N, Dunn RJ, Maler L. Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J Neurophysiol 86: 1612-1621, 2001. (Pubitemid 32953212)
6. Bloodgood BL, Sabatini BL. Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53: 249-260, 2007.
7. Borst A, Egelhaaf M. Principles of visual motion detection. Trends Neurosci 12: 297-306, 1989.
8. Borst A, Egelhaaf M. Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. Proc Natl Acad Sci USA 87: 9363-9367, 1990. (Pubitemid 120030626)
9. Carver S, Roth E, Cowan NJ, Fortune ES. Synaptic plasticity can produce and enhance direction selectivity. PLoS Comput Biol 4: e32, 2008. (Pubitemid 351328508)
10. Chacron MJ. Nonlinear information processing in a model sensory system. J Neurophysiol 95: 2933-2946, 2006.
11. Chacron MJ, Bastian J. Population coding by electrosensory neurons. J Neurophysiol 99: 1825-1835, 2008.
12. Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423: 77-81, 2003. (Pubitemid 36569585)
13. Chacron MJ, Toporikova N, Fortune ES. Differences in the time course of short-term depression across receptive fields are correlated with directional selectivity in electrosensory neurons. J Neurophysiol 102: 3270-3279, 2009.
14. Chance FS, Nelson SB, Abbott LF. Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18: 4785-4799, 1998.
15. Coulter DA, Huguenard JR, Prince DA. Calcium currents in rat thalamocortical relay neurones: kinetic properties of the transient, low-threshold current. J Physiol 414: 587-604, 1989.
16. Cowan NJ, Fortune ES. The critical role of locomotion mechanics in decoding sensory systems. J Neurosci 27: 1123-1128, 2007.
17. Dhingra NK, Freed MA, Smith RG. Voltage-gated sodium channels improve contrast sensitivity of a retinal ganglion cell. J Neurosci 25: 8097-8103, 2005.
18. Euler T, Detwiler PB, Denk W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852, 2002. (Pubitemid 34966298)
19. Fortune ES. The decoding of electrosensory systems. Curr Opin Neurobiol 16: 474-480, 2006.
20. Fortune ES, Rose GJ. Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons in vivo. J Neurosci 17: 3815-3825, 1997.
21. Fortune ES, Rose GJ. Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information. J Neurosci 20: 7122-7130, 2000.
22. + channels enhance the temporal filtering properties of electrosensory neurons in the torus. J Neurophysiol 90: 924-929, 2003.
23. Fuzessery ZM, Hall JC. Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76: 1059-1073, 1996.
24. Fuzessery ZM, Richardson MD, Coburn MS. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J Neurophysiol 96: 1320-1336, 2006. (Pubitemid 44371524)
25. Giffin K, Solomon JS, Burkhalter A, Nerbonne JM. Differential expression of voltage-gated calcium channels in identified visual cortical neurons. Neuron 6: 321-332, 1991.
26. Haag J, Borst A. Amplification of high-frequency synaptic inputs by active dendritic membrane processes. Nature 379: 639-641, 1996. (Pubitemid 26052824)
27. Haag J, Denk W, Borst A. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc Natl Acad Sci USA 101: 16333-16338, 2004. (Pubitemid 39552845)
28. Heckman CJ, Lee RH, Brownstone RM. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26: 688-695, 2003.
29. Hitschfeld ÉM, Stamper SA, Vonderschen K, Fortune ES, Chacron MJ. Effects of restraint and immobilization on electrosensory behaviors of weakly electric fish ILAR J 50: 361-372, 2009.
30. Hubel DH, Wiesel TN. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160: 106-154, 1962.
31. Inomata N, Tokutomi N, Oyama Y, Akaike N. Intracellular picrotoxin blocks pentobarbital-gated chloride conductance. Neurosci Res 6: 72-75, 1988.
32. Jagadeesh B, Wheat HS, Kontsevich LL, Tyler CW, Ferster D. Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J Neurophysiol 78: 2772-2789, 1997. (Pubitemid 27495501)
33. Johnston SA, Maler L, Tinner B. The distribution of serotonin in the brain of Apteronotus leptorhynchus: an immunohistochemical study. J Chem Neuroanat 3: 429-465, 1990.
34. Maler L, Sas E, Johnston S, Ellis W. An atlas of the brain of the weakly electric fish Apteronotus Leptorhynchus. J Chem Neuroanat 4: 1-38, 1991.
35. Mehaffey WH, Ellis LD, Krahe R, Dunn RJ, Chacron MJ. Ionic and neuromodulatory regulation of burst discharge controls frequency tuning. J Physiol 102: 195-208, 2008.
36. Mehrke G, Zong XG, Flockerzi V, Hofmann F. The Ca(++)-channel blocker Ro 40-5967 blocks differently T-type and L-type Ca++ channels. J Pharmacol Exp Therap 271: 1483-1488, 1994.
37. Nelson ME, MacIver MA. Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202: 1195-1203, 1999.
38. Priebe NJ, Ferster D. Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57: 482-497, 2008. (Pubitemid 351274000)
39. Priebe NJ, Mechler F, Carandini M, Ferster D. The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nat Neurosci 7: 1113-1122, 2004. (Pubitemid 41184452)
40. Ramcharitar JU, Tan EW, Fortune ES. Effects of global electrosensory signals on motion processing in the midbrain of Eigenmannia. J Comp Physiol A Sens Neural Behav Physiol 191: 865-872, 2005.
41. Ramcharitar JU, Tan EW, Fortune ES. Global electrosensory oscillations enhance directional responses of midbrain neurons in Eigenmannia. J Neurophysiol 96: 2319-2326, 2006.
42. Razak KA, Fuzessery ZM. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96: 1303-1319, 2006. (Pubitemid 44371523)
43. Razak KA, Fuzessery ZM. Facilitatory mechanisms underlying selectivity for the direction and rate of frequency modulated sweeps in the auditory cortex. J Neurosci 28: 9806-9816, 2008.
44. Reichardt W. editor. Movement Perception in Insects. New York: Academic, 1969.
45. Reichardt W. Evaluation of optical motion information by movement detectors. J Comp Physiol [A] 161: 533-547, 1987.
46. Reichardt W, Wenking H. Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56: 424-425, 1969.
47. Rhodes P. The properties and implications of NMDA spikes in neocortical pyramidal cells. J Neurosci 26: 6704-6715, 2006. (Pubitemid 44315232)
48. Rose GJ, Fortune ES. New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26: 89-94, 1996.
49. Rush ME, Rinzel J. Analysis of bursting in a thalamic neuron model. Biol Cybern 71: 281-291, 1994.
50. 2+ channels share NMDA receptors in plasticity of synaptic transmission in the rat visual cortex? Neuroreport 11: 3887-3891, 2000.
51. Schwindt PC, Crill WE. Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74: 2220-2224, 1995.
52. Srinivasan MV, Poteser M, Kral K. Motion detection in insect orientation and navigation. Vision Res 39: 2749-2766, 1999. (Pubitemid 29249084)
53. Suga N. Analysis of frequency-modulated sounds by auditory neurons of echo-locating bats. J Physiol 179: 26-53, 1965.
54. 2+ currents in the primary sensory neurons of Xenopus larvae. J Neurosci 17: 6839-6849, 1997.
55. Toporikova N, and Chacron MJ. Dendritic SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. J Neurophysiol 102: 2273-2287, 2009.
56. Turner RW, Maler L, Deerinck T, Levinson SR, Ellisman MH. TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J Neurosci 14: 6453-6471, 1994. (Pubitemid 24333067)