Differences in the time course of short-term depression across receptive fields are correlated with directional selectivity in electrosensory neurons

Journal of Neurophysiology

Volumn 102, Issue 6, 2009, Pages 3270-3279

  Chacron, Maurice J ^a   Toporikova, Natalia ^a   Fortune, Eric S ^b  

^a MCGILL UNIVERSITY   (Canada)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DIRECTIONAL SELECTIVITY; ELECTRIC FISH; INFERIOR COLLICULUS; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RECEPTIVE FIELD; SENSORY NERVE CELL; SHORT TERM DEPRESSION; SYNAPTIC TRANSMISSION; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; ELECTRIC FISH; ELECTRIC ORGAN; ELECTRIC STIMULATION; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NEURAL INHIBITION; ORIENTATION; REACTION TIME; SENSORY RECEPTOR CELLS; TIME FACTORS; VISUAL FIELDS;

EID: 72749102952     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00645.2009     Document Type: Article

References (51)

1. Adelson EH, Bergen JR. Spatiotemporal energy models for the perception of motion. J Opt Soc Am A Opt Image Sci Vis 2: 284-299, 1985.
2. 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 Sens Neural Behav Physiol 144: 481-494, 1981.
3. 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)
4. Borst A. Correlation versus gradient type motion detectors: the pros and cons. Philos Trans R Soc Lond B Biol Sci 362: 369-374, 2007. (Pubitemid 47056842)
5. Borst A, Egelhaaf M. Principles of visual motion detection. Trends Neurosci 12: 297-306, 1989.
6. Boudreau CE, Ferster D. Short-term depression in thalamocortical synapses of cat primary visual cortex. J Neurosci 25: 7179-7190, 2005. (Pubitemid 41113934)
7. Carr CE, Maler L. A Golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: functional and morphological diversity in the midbrain. J Comp Neurol 235: 207-240, 1985. (Pubitemid 15051652)
8. Carver S, Roth E, Cowan NJ, Fortune ES. Synaptic plasticity can produce and enhance direction selectivity. PLoS Comput Biol 4: e32, 2008.
9. Chacron MJ. Nonlinear information processing in a model sensory system. J Neurophysiol 95: 2933-2946, 2006.
10. Chacron MJ, Bastian J. Population coding by electrosensory neurons. J Neurophysiol 99: 1825-1835, 2008.
11. 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)
12. Chacron MJ, Maler L, Bastian J. Feedback and feedforward control of frequency tuning to naturalistic stimuli. J Neurosci 25: 5521-5532, 2005. (Pubitemid 40800644)
13. Chance FS, Nelson SB, Abbott LF. Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18: 4785-4799, 1998.
14. Cowan NJ, Fortune ES. The critical role of locomotion mechanics in decoding sensory systems. J Neurosci 27: 1123-1128, 2007.
15. Fortune ES. The decoding of electrosensory systems. Curr Opin Neurobiol 16: 474-480, 2006.
16. Fortune ES, Rose GJ. Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information. J Neurosci 20: 7122-7130, 2000. (Pubitemid 30708042)
17. Frank K, Becker MC. Microelectrodes for recording and stimulation. In: Physical Techniques in Biological Research, Part A. New York: Academic, 1964, p. 23-84.
18. 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.
19. 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)
20. Heiligenberg W. Neural Nets in Electric Fish. Cambridge, MA: MIT Press, 1991.
21. Hitschfeld ÉM, Stamper SA, Vonderschen K, Fortune ES, Chacron MJ. Effects of restraint and immobilization on electrosensory behaviors of weakly electric fish. ILAR Journal 50: 361-372, 2009.
22. Hubel D. Single unit activity in striate cortex of unrestrained cats. J Physiol 147: 226-238, 1959.
23. Hubel DH, Wiesel TN. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160: 106-154, 1962.
24. Jagadeesh B, Wheat HS, Ferster D. Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. Science 262: 1901-1904, 1993.
25. 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)
26. Krahe R, Bastian J, Chacron MJ. Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 100: 852-867, 2008.
27. MacIver MA, Sharabash NM, Nelson ME. Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204: 543-557, 2001.
28. Maler L. The posterior lateral line lobe of certain gymnotiform fish. Quantitative light microscopy. J Comp Neurol 183: 323-363, 1979.
29. 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.
30. Maler L, Sas EK, Rogers J. The cytology of the posterior lateral line lobe of high frequency weakly electric fish (Gymnotoidei): differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195: 87-139, 1981. (Pubitemid 11122573)
31. 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.
32. Newbold P. Statistics for Business and Economics. Englewood Cliffs, NJ: Prentice Hall, 2006, p. 984.
33. Priebe NJ, Ferster D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45: 133-145, 2005. (Pubitemid 40075355)
34. Priebe NJ, Ferster D. Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57: 482-497, 2008. (Pubitemid 351274000)
35. 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.
36. Ramcharitar JU, Tan EW, Fortune ES. Global electrosensory oscillations enhance directional responses of midbrain neurons in Eigenmannia. J Neurophysiol 96: 2319-2326, 2006.
37. 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)
38. 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.
39. Reichardt W. Editor. Movement Perception in Insects. New York: Academic Press, 1969.
40. Reichardt W. Evaluation of optical motion information by movement detectors. J Comp Physiol A Sens Neural Behav Physiol 161: 533-547, 1987.
41. Rose GJ, Fortune ES. New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26: 89-94, 1996.
42. Rose GJ, Fortune ES. Frequency-dependent PSP depression contributes to low-pass temporal filtering in Eigenmannia. J Neurosci 19: 7629-7639, 1999.
43. Shumway C. Multiple electrosensory maps in the medulla of weakly electric Gymnotiform fish. I. Physiological differences. J Neurosci 9: 4388-4399, 1989a. (Pubitemid 20027253)
44. Shumway C. Multiple electrosensory maps in the medulla of weakly electric Gymnotiform fish. II. Anatomical differences. J Neurosci 9: 4400-4415, 1989b. (Pubitemid 20027254)
45. Sillito AM, Kemp JA, Blakemore C. The role of GABAergic inhibition in the cortical effects of monocular deprivation. Nature 291: 318-320, 1981. (Pubitemid 11083427)
46. Suga N. Responses of cortical auditory neurones to frequency modulated sounds in echo-locating bats. Nature 206: 890-891, 1965.
47. Taylor WR, He S, Levick WR, Vaney DI. Dendritic computation of direction selectivity by retinal ganglion cells. Science 289: 2347-2350, 2000. (Pubitemid 30739738)
48. Toporikova N, Chacron MJ. Dendritic SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. J Neurophysiol (August 12, 2009). doi:10.1152/jn.00282.2009.
49. Turner RW, Maler L, Burrows M. Electroreception and electrocommunication. J Exp Biol 202: 1167-1458, 1999.
50. Varela JA, Sen K, Gibson J, Frost J, Abbott LF, Nelson SB. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17: 7926-7940, 1997. (Pubitemid 27426228)
51. Yang G, Masland RH. Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258: 1949-1952, 1992.