Statistics of the vestibular input experienced during natural self-motion: Implications for neural processing

Journal of Neuroscience

Volumn 34, Issue 24, 2014, Pages 8347-8357

  Carriot, Jerome ^a   Jamali, Mohsen ^a   Chacron, Maurice J ^a   Cullen, Kathleen E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Natural stimuli; Power law; Preneuronal processing

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CENTRAL NERVOUS SYSTEM FUNCTION; EXPERIMENTAL STUDY; FEMALE; HEAD MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; METHODOLOGY; MOTOR PERFORMANCE; NERVE POTENTIAL; NEURAL PROCESSING; NORMAL HUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SENSORY NERVE CONDUCTION; SIGNAL TRANSDUCTION; TASK PERFORMANCE; VESTIBULAR FUNCTION;

NATURAL STIMULI; POWER LAW; PRENEURONAL PROCESSING;

ADULT; EFFERENT PATHWAYS; FEMALE; HEAD MOVEMENTS; HUMANS; MALE; MODELS, BIOLOGICAL; MOTION; MOTION PERCEPTION; PHYSICAL STIMULATION; PROPRIOCEPTION; PSYCHOPHYSICS; REFLEX, VESTIBULO-OCULAR; SPECTRUM ANALYSIS; VESTIBULE, LABYRINTH; YOUNG ADULT;

EID: 84902167922     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0692-14.2014     Document Type: Article

References (70)

1. Anderson JR (1990) The adaptive character of thought. Hillsdale, NJ: Erlbaum.
2. Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125-150. CrossRef Medline
3. Attias H, Schreiner CE (1998) Blind source separation and deconvolution: the dynamic component analysis algorithm. Neural Comput 10:1373-1424. CrossRef Medline
4. Attneave F (1954) Some informational aspects of visual perception. Psychol Rev 61:183-193. CrossRef Medline
5. Baird RA, Desmadryl G, Fernández 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. Medline
6. Barlow H (2001) Redundancy reduction revisited. Network 12:241-253. CrossRef Medline
7. Barlow HB, Narasimhan R, Rosenfeld A (1972) Visual pattern analysis in machines and animals. Science 177:567-575. CrossRef Medline
8. Borghuis BG, Ratliff CP, Smith RG, Sterling P, Balasubramanian V (2008) Design of a neuronal array. J Neurosci 28:3178-3189. CrossRef Medline
9. Brannon EM, Libertus ME, Meck WH, Woldorff MG (2008) Electrophysiological measures of time processing in infant and adult brains: Weber's Law holds. J Cogn Neurosci 20:193-203. CrossRef Medline
10. Bril B, Ledebt A (1998) Head coordination as a means to assist sensory integration in learning to walk. Neurosci Biobehav Rev 22:555-563. CrossRef Medline
11. Burton GJ, Moorhead IR (1987) Color and spatial structure in natural scenes. Appl Opt 26:157-170. CrossRef Medline
12. Chater N, Brown GD (1999) Scale-invariance as a unifying psychological principle. Cognition 69:B17-B24. CrossRef Medline
13. 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. CrossRef Medline
14. Cromwell RL, Newton RA, Forrest G (2002) Influence of vision on head stabilization strategies in older adults during walking. J Gerontol A Biol Sci Med Sci 57:M442-M448. CrossRef Medline
15. Cromwell RL, Pidcoe PE, Griffin LA, Sotillo T, Ganninger D, Feagin M (2004a) Adaptations in horizontal head stabilization in response to altered vision and gaze during natural walking. J Vestib Res 14:367-373. Medline
16. Cromwell R, Schurter J, Shelton S, Vora S (2004b) Head stabilization strategies in the sagittal plane during locomotor tasks. Physiother Res 9:33-42. CrossRef Medline
17. Cullen KE (2011) The neural encoding of self-motion. Curr Opin Neurobiol 21:587-595. CrossRef Medline
18. Cullen KE (2012) The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci 35:185-196. CrossRef Medline
19. Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919-1933. CrossRef Medline
20. De Coensel B, Botteldooren D, De Muer T (2003) 1/f noise in rural and urban soundscapes. Acta Acust United Ac 89:287-295.
21. Dehaene S (2003) The neural basis of the Weber-Fechner law: a logarithmic mental number line. Trends Cogn Sci 7:145-147. CrossRef Medline
22. Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CTreconstruction. J Assoc Res Otolaryngol 6:191-206. CrossRef Medline
23. Doi E, Gauthier JL, Field GD, Shlens J, Sher A, Greschner M, Machado TA, Jepson LH, Mathieson K, Gunning DE, Litke AM, Paninski L, Chichilnisky EJ, Simoncelli EP (2012) Efficient coding of spatial information in the primate retina. J Neurosci 32:16256-16264. CrossRef Medline
24. Dong DW, Atick JJ (1995) Temporal decorrelation: a theory of lagged and nonlagged responses in the lateral geniculate-nucleus. Netw Comp Neural 6:159-178. CrossRef
25. Fernández C, Goldberg JM (1971) 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. Medline
26. Fernández 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. Medline
27. Field DJ (1987) Relations between the statistics of natural images and the response properties of cortical cells. J Opt Soc Am A 4:2379-2394. CrossRef Medline
28. Francisco E, Tannan V, Zhang Z, Holden J, Tommerdahl M (2008) Vibrotactile amplitude discrimination capacity parallels magnitude changes in somatosensory cortex and follows Weber's Law. Exp Brain Res 191:49-56. CrossRef Medline
29. Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277-297. CrossRef Medline
30. Hinz B, Menzel G, Blüthner R, Seidel H (2010) Seat-to-head transfer function of seated men: determination with single and three axis excitations at different magnitudes. Industrial Health 48:565-583. CrossRef Medline
31. Hullar TE, Della Santina CC, Hirvonen T, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777-2786. CrossRef Medline
32. Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during highfrequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88:13-28. Medline
33. Jamali M, Carriot J, Chacron MJ, Cullen KE (2013) Strong correlations between sensitivity and variability give rise to constant discrimination thresholds across the otolith afferent population. J Neurosci 33:11302-11313. CrossRef Medline
34. Jones GM, Spells KE (1963) A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc R Soc Lond B Biol Sci 157:403-419. CrossRef Medline
35. Kuang X, Poletti M, Victor JD, Rucci M (2012) Temporal encoding of spatial information during active visual fixation. Curr Biol 22:510-514. CrossRef Medline
36. Laming D (1986) Sensory analysis. London: Academic.
37. Lasker DM, Han GC, Park HJ, Minor LB (2008) Rotational responses of vestibular-nerve afferents innervating the semicircular canals in the C57BL/6 mouse. J Assoc Res Otolaryngol 9:334-348. CrossRef Medline
38. Laughlin S (1981) A simple coding procedure enhances a neuron's information capacity. Z Naturforsch C 36:910-912. Medline
39. Lewen GD, Bialek W, de Ruyter van Steveninck RR (2001) Neural coding of naturalistic motion stimuli. Network 12:317-329. CrossRef Medline
40. Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AV (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21:3215-3227. Medline
41. Mallery RM, Olomu OU, Uchanski RM, Militchin VA, Hullar TE (2010) Human discrimination of rotational velocities. Exp Brain Res 204:11-20. CrossRef Medline
42. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME (2007) Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. Plo S Biol 5:e19. CrossRef Medline
43. Massot C, Chacron MJ, Cullen KE (2011) Information transmission and detection thresholds in the vestibular nuclei: single neurons vs. population encoding. J Neurophysiol 105:1798-1814. CrossRef Medline
44. Massot C, Schneider AD, Chacron MJ, Cullen KE (2012) The vestibular system implements a linear-nonlinear transformation in order to encode self-motion. Plos Biol 10:e1001365. CrossRef Medline
45. McMahon TA (1984) Muscles, reflexes, and locomotion. Princeton, NJ: Princeton UP.
46. Merigan WH, Maunsell JH (1993) How parallel are the primate visual pathways? Annu Rev Neurosci 16:369-402. CrossRef Medline
47. 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. Medline
48. Moore JD, Deschênes M, Furuta T, Huber D, Smear MC, Demers M, Kleinfeld D (2013) Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497:205-210. CrossRef Medline
49. Nigg BM, Liu W (1999) The effect of muscle stiffness and damping on simulated impact force peaks during running. J Biomech 32:849-856. CrossRef Medline
50. Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61:497-519. CrossRef Medline
51. Pozzo T, Berthoz A, Lefort L, Vitte E (1991a) Head stabilization during various locomotor tasks in humans: II. Patients with bilateral peripheral vestibular deficits. Exp Brain Res 85:208-217. Medline
52. Pozzo T, Berthoz A, Vitte E, Lefort L (1991b) Head stabilization during locomotion: perturbations induced by vestibular disorders. Acta Otolaryngol Suppl 481:322-327. Medline
53. Puchalla JL, Schneidman E, Harris RA, Berry MJ (2005) Redundancy in the population code of the retina. Neuron 46:493-504. CrossRef Medline
54. Rieke F, Bodnar DA, Bialek W (1995) Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc Biol Sci 262:259-265. CrossRef Medline
55. Ruderman DL, Bialek W (1994) Statistics of natural images: scaling in the woods. Phys Rev Lett 73:814-817. CrossRef Medline
56. Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE (2007) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27:771-781. CrossRef Medline
57. Schneidman E, Berry MJ 2nd, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012. CrossRef Medline
58. Shepard RN (1987) Toward a universal law of generalization for psychological science. Science 237:1317-1323. CrossRef Medline
59. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193-1216. CrossRef Medline
60. Spoor F, Bajpai S, Hussain ST, Kumar K, Thewissen JG (2002) Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417:163-166. CrossRef Medline
61. Tkacik G, Prentice JS, Balasubramanian V, Schneidman E (2010) Optimal population coding by noisy spiking neurons. Proc Natl Acad Sci U S A 107:14419-14424. CrossRef Medline
62. Tolhurst DJ, Tadmor Y, Chao T (1992) Amplitude spectra of natural images. Ophthalmic Physiol Opt 12:229-232. Medline
63. Vinje WE, Gallant JL (2002) Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. J Neurosci 22:2904-2915. Medline
64. Wakeling JM, Nigg BM, Rozitis AI (2002) Muscle activity damps the soft tissue resonance that occurs in response to pulsed and continuous vibrations. J Appl Physiol 93:1093-1103. CrossRef Medline
65. Wakeling JM, Liphardt AM, Nigg BM (2003) Muscle activity reduces softtissue resonance at heel-strike during walking. J Biomech 36:1761-1769. CrossRef Medline
66. Wallman J, Velez J, Weinstein B, Green AE (1982) Avian vestibuloocular reflex: adaptive plasticity and developmental changes. J Neurophysiol 48: 952-967. Medline
67. Yang A, Hullar TE (2007) Relationship of semicircular canal size to vestibular-nerve afferent sensitivity in mammals. J Neurophysiol 98: 3197-3205. CrossRef Medline
68. Zanker JM (1996) On the elementary mechanism underlying secondary motion processing. Philos Trans R Soc Lond B Biol Sci 351:1725-1736. CrossRef Medline
69. Zatiorsky VM (1998) Kinematic of human motion, human kinetics edition. New York: Human Kinetics.
70. Zhaoping L (2006) Theoretical understanding of the early visual processes by data compression and data selection. Network 17:301-334. CrossRef Medline