Neural variability, detection thresholds, and information transmission in the vestibular system

Journal of Neuroscience

Volumn 27, Issue 4, 2007, Pages 771-781

  Sadeghi, Soroush G ^a   Chacron, Maurice J ^a   Taylor, Michael C ^a   Cullen, Kathleen E ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b Aerospace Medical Research Unit   (Canada)

Author keywords

Detection threshold; Heterogeneity; Information theory; Regular afferents; Spike timing; Vestibular afferents

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HEAD MOVEMENT; INFORMATION PROCESSING; NERVE CELL; NERVOUSNESS; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SENSORY STIMULATION; SENSORY SYSTEM; SIGNAL NOISE RATIO; SPIKE WAVE; VESTIBULAR SYSTEM;

ACTION POTENTIALS; ANIMALS; DIFFERENTIAL THRESHOLD; HEAD MOVEMENTS; MACACA FASCICULARIS; NEURONS; SYNAPTIC TRANSMISSION; VESTIBULE;

EID: 33846605614     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4690-06.2007     Document Type: Article

References (78)

1. Adrian E, Zotterman Y (1926) The impulses produced by sensory nerve endings. Part 3. Impulses set up by touch and pressure. J Physiol (Lond) 61:465-483.
2. Andreasen M, Lambert JD (1999) Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones. J Physiol (Lond) 519:85-100.
3. Armand M, Minor LB (2001) Relationship between time- and frequency-domain analyses of angular head movements in the squirrel monkey. J Comput Neurosci 11:217-239.
4. Bacsi AM, Colebatch JG (2005) Evidence for reflex and perceptual vestibular contributions to postural control. Exp Brain Res 160:22-28.
5. Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182-203.
6. Becker W, Jurgens R, Boss T (2000) Vestibular perception of self-rotation in different postures: a comparison between sitting and standing subjects. Exp Brain Res 131:468-476.
7. Benson AJ, Hutt EC, Brown SF (1989) Thresholds for the perception of whole body angular movement about a vertical axis. Aviat Space Environ Med 60:205-213.
8. Beraneck M, Hachemaoui M, Idoux E, Ris L, Uno A, Godaux E, Vidal PP, Moore LE, Vibert N (2003) Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy. J Neurophysiol 90:184-203.
9. Berman NJ, Maler L (1998) Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J Neurophysiol 80:3214-3232.
10. Borst A, Haag J (2001) Effects of mean firing on neural information rate. J Comp Neurosci 10:213-221.
11. Carr CE (1993) Processing of temporal information in the brain. Annu Rev Neurosci 16:223-243.
12. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227-3246.
13. Chacron MJ (2006) Nonlinear information processing in a model sensory system. J Neurophysiol 95:2933-2946.
14. Chacron MJ, Longtin A, St-Hilaire M, Maler L (2000) Suprathreshold stochastic firing dynamics with memory in P-type electroreceptors. Phys Rev Lett 85:1576-1579.
15. Chacron MJ, Longtin A, Maler L (2001) Negative interspike interval correlations increase the neuronal capacity for encoding time-varying stimuli. J Neurosci 21:5328-5343.
16. Chacron MJ, Pakdaman K, Longtin A (2003) Interspike interval correlations, memory, adaptation, and refractoriness in a leaky integrate-and-fire model with threshold fatigue. Neural Comput 15:253-278.
17. Chacron MJ, Lindner B, Longtin A (2004) Noise shaping by interval correlations increases information transfer. Phys Rev Lett 92:080601.
18. Chacron MJ, Maler L, Bastian J (2005a) Electroreceptor neuron dynamics shape information transmission. Nat Neurosci 8:673-678.
19. Chacron MJ, Maler L, Bastian J (2005b) Feedback and feedforward control of frequency tuning to naturalistic stimuli. J Neurosci 25:5521-5532.
20. Chacron MJ, Longtin A, Maler L (2005c) Delayed excitatory and inhibitory feedback shape neural information transmission. Phys Rev E Stat Nonlin Soft Matter Phys 72:051917.
21. Chen-Huang C, McCrea RA, Goldberg JM (1997) Contributions of regularly and irregularly discharging vestibular-nerve inputs to the discharge of central vestibular neurons in the alert squirrel monkey. Exp Brain Res 114:405-422.
22. Connor CE, Hsiao SS, Phillips JR, Johnson KO (1990) Tactile roughness: neural codes that account for psychophysical magnitude estimates. J Neurosci 12:3823-3826.
23. Cox DR, Lewis PA (1966) The statistical analysis of series of events. London: Methuen.
24. Crill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362.
25. Cullen KE, Minor LB (2002) Semicircular canal afferents similarly encode active and passive head-on body rotations: implications for the role of vestibular efference. J Neurosci 22:RC226.
26. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, MA: MIT.
27. Eatock RA, Hurley KM (2003) Functional development of hair cells. Curr Top Dev Biol 57:389-448.
28. Eatock RA, Hurley KM, Vollrath MA (2002) Mechanoelectrical and voltage-gated ion channels in mammalian vestibular hair cells. Audiol Neurootol 7:31-35.
29. Fernandez C, Baird RA, Goldberg JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. J Neurophysiol 60:167-181.
30. Fitzpatrick R, McCloskey DI (1994) Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol (Lond) 478:173-186.
31. Gabbiani F (1996) Coding of time varying signals in spike trains of linear and half-wave rectifying neurons. Network 7:61-85.
32. Goldberg JM (2000) Afferent diversity and the organisation of central vestibular pathways. Exp Brain Res 130:277-297.
33. Goldberg JM, Fernández C (1971a) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular acceleration. J Neurophysiol 34:635-660.
34. Goldberg JM, Fernandez C (1971b) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661-675.
35. Goldberg JM, Smith CE, Fernandez C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51:1236-1256.
36. Green D, Swets J (1966) Signal detection theory and psychophysics. New York: Wiley.
37. Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470-476.
38. Haque A, Angelaki DE, Dickman JD (2004) Spatial tuning and dynamics of vestibular semicircular afferents in rhesus monkeys. Exp Brain Res 155:81-90.
39. Hullar TE, Minor LB (1999) High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. J Neurophysiol 82:2000-2005.
40. Hullar TE, Della Santina CC, Hirvonen T, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla simicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777-2786.
41. + currents in type I hair cells and calyx afferent endings of the developing rat utricle. J Neurosci 26:10253-10269.
42. Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88:13-28.
43. Jarvis MR, Mitra PP (2001) Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput 13:717-749.
44. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7:170-177.
45. Johnston AR, MacLeod NK, Dutia MB (1994) Ionic conductances contributing to spike repolarisation and after-potentials in rat medial vestibular nucleus neurons. J Physiol (Lond) 481:61-77.
46. Jones LM, Depireux DA, Simons DJ, Keller A (2004) Robust temporal coding in the trigeminal system. Science 304:1986-1989.
47. Joseph A, Hyson R (1993) Coincidence detection by binaural neurons in the chick brain stem. J Neurophysiol 69:1197-1211.
48. Jurgens R, Becker W (2006) Perception of angular displacement without landmarks: evidence for Bayesian fusion of vestibular, optokinetic, podokinesthetic, and cognitive information. Exp Brain Res 174:528-543.
49. Kreiman G, Krahe R, Metzner W, Koch C, Gabbiani F (2000) Robustness and variability of neuronal coding by amplitude sensitive afferents in the weakly electric fish Eigenmania. J Neurophysiol 84:189-224.
50. Laurent G, Davidowitz H (1994) Encoding of Olfactory Information with Oscillating Neural Assemblies. Science 265:1872-1875.
51. +-currents density is correlated with soma size in rat vestibular-afferent neurons in culture. J Neurophysiol 94:3751-3761.
52. 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 Stat Nonlin Soft Matter Phys 72:021911.
53. Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346-354.
54. Liu YH, Wang XJ (2001) Spike frequency adaptation of a generalized leaky integrate-and-fire neuron. J Comp Neurosci 10:25-45.
55. Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AV (2001) Representation of acoustic communication signals by insect auditory neurons. J Neurosci 21:3215-3227.
56. Meister M (1996) Multineuronal codes in retinal signaling. Proc Natl Acad Sci USA 93:609-614.
57. Mergner T, Hlavacka F, Schweigart G (1993) Interaction of vestibular and proprioceptive inputs. J Vestib Res 3:41-57.
58. Minor LB, Goldberg JM (1991) Vestibular-nerve inputs to the vestibuloocular reflex: a functional-ablation study in the squirrel monkey. J Neurosci 11:1636-1648.
59. Oppenheim AV, Schafer RW (1989) Discrete-time signal processing. Englewood Cliffs, NJ: Prentice Hall.
60. Ramachandran R, Lisberger SG (2006) Transformation of vestibular signals into motor commands in the vestibuloocular reflex pathways of monkeys. J Neurophysiol 96:1061-1074.
61. Richmond BJ, Optican LM, Podell M, Spitzer H (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. J Neurophysiol 57:132-146.
62. Rieke F, Warland D, de Ruyter van Steveninck RR, Bialek W (1996) Spikes: exploring the neural code. Cambridge, MA: MIT.
63. Roddey JC, Girish B, Miller JP (2000) Assessing the performance of neural encoding models in the presence of noise. J Comp Neurosci 8:95-112.
64. Romer A, Parsons TS (1977) The vertebrate body. Philadelphia: Saunders.
65. Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131-2142.
66. Sadeghi SG, Minor LB, Cullen KE (2006) Response of vestibular-nerve afferents to active and passive rotations under normal conditions and following unilateral labyrinthectomy. J Neurophysiol, in press.
67. Salinas E, Hernandez A, Zainos A, Romo R (2000) Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli. J Neurosci 20:5503-5515.
68. Schessel DA (1982) Chemical synaptic transmission between type I vestibular hair cells and the primary afferent nerve chalice: an intracellular study utilizing horseradish peroxidase. PhD thesis, Albert Einstein College of Medicine, Bronx, NY.
69. Schessel DA, Ginzberg R, Highstein SM (1991) Morphophysiology of synaptic transmission between type I hair cells and vestibular primary afferents. An intracellular study employing horseradish peroxidase in the lizard, Calotes versicolor. Brain Res 544:1-16.
70. Smith CE, Goldberg JM (1986) A stochastic afterhyperpolarization model of repetitive activity in vestibular afferents. Biol Cybern 41-51.
71. Snippe HP, Koenderink JJ (1992) Discrimination thresholds for channel-coded systems. Biol Cybern 66:543-551.
72. Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal. Nat Rev Neurosci 6:4766-4778.
73. Straka H, Vibert N, Vidal PP, Moore LE, Dutia MB (2005) Intrinsic membrane properties of vertebrate vestibular neurons: function, development, and plasticity. Prog Neurobiol 76:349-392.
74. Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15:1065-1076.
75. Sylvestre PA, Cullen KE (1999) Quantitative analysis of abducens neuron discharge dynamics during saccadic and slow eye movements. J Neurophysiol 82:2612-2632.
76. Tasaki I (1955) New measurements of the capacity and resistance of the myelin sheath and the nodal membrane of the isolated frog nerve fiber. Am J Physiol 181:639-650.
77. Theunissen F, Miller JP (1995) Temporal encoding in the nervous system: a rigorous definition. J Comput Neurosci 2:149-162.
78. Theunissen F, Roddey JC, Stufflebeam S, Clague H, Miller JP (1996) Information theoretic analysis of dynamical encoding by four identified interneurons in the cricket cercal system. J Neurophysiol 75:1345-1364.