Speed-invariant encoding of looming object distance requires power law spike rate adaptation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages 13624-13629

  Clarke, Stephen E ^a   Naud, Richard ^b   Longtin, André ^a,b   Maler, Leonard ^a  

^a Departments of Cellular and Molecular Medicine   (United States)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Neural coding; Perceptual invariance; Sensory transformations; Spike frequency adaptation

Indexed keywords

ACCELERATION; ADAPTATION; ANIMAL BEHAVIOR; ANIMAL CELL; APTERONOTUS LEPTORHYNCHUS; ARTICLE; BIOPHYSICS; DISTANCE PERCEPTION; ELECTRIC CONDUCTIVITY; ELECTRIC FISH; ELECTRIC POTENTIAL; ELECTRORECEPTOR; MEMBRANE POTENTIAL; NEGATIVE FEEDBACK; NERVE CELL; NONHUMAN; ORIENTING RESPONSE; PRIORITY JOURNAL; SENSORY NERVE CELL; SPIKE; STIMULUS; SYNAPSE; VELOCITY;

NEURAL CODING; PERCEPTUAL INVARIANCE; SENSORY TRANSFORMATIONS; SPIKE FREQUENCY ADAPTATION;

ANIMALS; CEREBELLUM; ELECTRIC CONDUCTIVITY; GYMNOTIFORMES; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURONS; TIME FACTORS;

EID: 84882393789     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306428110     Document Type: Article

References (50)

1. Purves D, Wojtach WT, Lotto RB (2011) Understanding vision in wholly empirical terms. Proc Natl Acad Sci USA 108(Suppl 3):15588-15595.
2. Fairhall AL, et al. (2006) Selectivity for multiple stimulus features in retinal ganglion cells. J Neurophysiol 96(5):2724-2738.
3. Gussin D, Benda J, Maler L (2007) Limits of linear rate coding of dynamic stimuli by electroreceptor afferents. J Neurophysiol 97(4):2917-2929.
4. Gabbiani F, Krapp HG, Laurent G (1999) Computation of object approach by a widefield, motion-sensitive neuron. J Neurosci 19(3):1122-1141.
5. Sun HJ, Frost BJ (1998) Computation of different optical velocities of looming objects. Nat Neurosci 1(4):296-303.
6. Heiligenberg W (1973) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87(2):137-164.
7. MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: Motion analysis and effects of water conductivity. J Exp Biol 204(3): 543-557.
8. Maler L (2009) Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 516(5): 376-393.
9. Chen L, House JL, Krahe R, Nelson ME (2005) Modeling signal and background components of electrosensory scenes. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191(4):331-345.
10. Chacron MJ, Longtin A, St-Hilaire M, Maler L (2000) Suprathreshold stochastic firing dynamics with memory in P-type electroreceptors. Phys Rev Lett 85(7):1576-1579.
11. Chacron MJ, Longtin A, Maler L (2001) Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimuli. J Neurosci 21(14): 5328-5343.
12. Knudsen EI (1974) Behavioral thresholds to electric signals in high frequency electric fish. J Comp Physiol 91(4):333-353.
13. Xu Z, Payne JR, Nelson ME (1996) Logarithmic time course of sensory adaptation in electrosensory afferent nerve fibers in a weakly electric fish. J Neurophysiol 76(3): 2020-2032.
14. Benda J, Longtin A, Maler L (2005) Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25(9):2312-2321.
15. Peron S, Gabbiani F (2009) Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12(3):318-326.
16. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54(4):782-806.
17. Benda J, Herz AV (2003) A universal model for spike-frequency adaptation. Neural Comput 15(11):2523-2564.
18. Drew PJ, Abbott LF (2006) Models and properties of power-law adaptation in neural systems. J Neurophysiol 96(2):826-833.
19. Wang XJ, Liu Y, Sanchez-Vives MV, McCormick DA (2003) Adaptation and temporal decorrelation by single neurons in the primary visual cortex. J Neurophysiol 89(6): 3279-3293.
20. French AS, Torkkeli PH (2008) The power law of sensory adaptation: Simulation by a model of excitability in spider mechanoreceptor neurons. Ann Biomed Eng 36(1): 153-161.
21. Wark B, Fairhall A, Rieke F (2009) Timescales of inference in visual adaptation. Neuron 61(5):750-761.
22. Lundstrom BN, Fairhall AL, Maravall M (2010) Multiple timescale encoding of slowly varying whisker stimulus envelope in cortical and thalamic neurons in vivo. J Neurosci 30(14):5071-5077.
23. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24(46):10440-10453.
24. Zilany MSA, Carney LH (2010) Power-law dynamics in an auditory-nerve model can account for neural adaptation to sound-level statistics. J Neurosci 30(31):10380-10390.
25. Laughlin SB (1989) The role of sensory adaptation in the retina. J Exp Biol 146(1): 39-62.
26. Lindner B, Chacron MJ, Longtin A (2005) Integrate-and-fire neurons with threshold noise: A tractable model of how interspike interval correlations affect neuronal signal transmission. Phys Rev E 72(2):021911.
27. Sobel EC, Tank DW (1994) In vivo Ca2+ dynamics in a cricket auditory neuron: An example of chemical computation. Science 263(5148):823-826.
28. Peron SP, Gabbiani F (2009) Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli. Biol Cybern 100(6):505-520.
29. Lundstrom BN, Higgs MH, Spain WJ, Fairhall AL (2008) Fractional differentiation by neocortical pyramidal neurons. Nat Neurosci 11(11):1335-1342.
30. Tripp BP, Eliasmith C (2010) Population models of temporal differentiation. Neural Comput 22(3):621-659.
31. Haykin S (2001) Communication Systems (Wiley, New York), pp 723-734.
32. Middleton JW, Longtin A, Benda J, Maler L (2006) The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc Natl Acad Sci USA 103(39):14596-14601.
33. Kohn A (2007) Visual adaptation: Physiology, mechanisms, and functional benefits. J Neurophysiol 97(5):3155-3164.
34. Zeng J, Powers RK, Newkirk G, Yonkers M, Binder MD (2005) Contribution of persistent sodium currents to spike-frequency adaptation in rat hypoglossal motoneurons. J Neurophysiol 93(2):1035-1041.
35. Baccus SA, Meister M (2002) Fast and slow contrast adaptation in retinal circuitry. Neuron 36(5):909-919.
36. Sokolove PG, Cooke IM (1971) Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J Gen Physiol 57(2):125-163.
37. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34(3): 437-446.
38. Liebovitch LS, Fischbarg J, Koniarek JP (1987) Ion channel kinetics: A model based on fractal scaling rather than multistate Markov processes. Math Biosci 84(1):37-68.
39. Millhauser GL, Salpeter EE, Oswald RE (1988) Diffusion models of ion-channel gating and the origin of power-law distributions from single-channel recording. Proc Natl Acad Sci USA 85(5):1503-1507.
40. Toib A, Lyakhov V, Marom S (1998) Interaction between duration of activity and time course of recovery from slow inactivation in mammalian brain Na+ channels. J Neurosci 18(5):1893-1903.
41. Torkkeli PH, French AS (2002) Simulation of different firing patterns in paired spider mechanoreceptor neurons: The role of Na(+) channel inactivation. J Neurophysiol 87(3):1363-1368.
42. Brenner N, Bialek W, de Ruyter van Steveninck R (2000) Adaptive rescaling maximizes information transmission. Neuron 26(3):695-702.
43. Panzeri S, Brunel N, Logothetis NK, Kayser C (2010) Sensory neural codes using multiplexed temporal scales. Trends Neurosci 33(3):111-120.
44. Chacron MJ (2006) Nonlinear information processing in a model sensory system. J Neurophysiol 95(5):2933-2946.
45. Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22(11):4577-4590.
46. Chacron MJ, Longtin A, Maler L (2011) Efficient computation via sparse coding in electrosensory neural networks. Curr Opin Neurobiol 21(5):752-760.
47. Nakagawa H, Hongjian K (2010) Collision-sensitive neurons in the optic tectum of the bullfrog, Rana catesbeiana. J Neurophysiol 104(5):2487-2499.
48. Trenholm S, Schwab DJ, Balasubramanian V, Awatramani GB (2013) Lag normalization in an electrically coupled neural network. Nat Neurosci 16(2):154-156.
49. Baker CL, Jr., Mareschal I (2001) Processing of second-order stimuli in the visual cortex. Prog Brain Res 134:171-191.
50. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84(2):541-577.