Whisker sensory system - From receptor to decision

Progress in Neurobiology

Volumn 103, Issue , 2013, Pages 28-40

  Diamond, Mathew E ^a   Arabzadeh, Ehsan ^b  

^a SISSA   (Italy)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Perception; Sensory coding; Sensory cortex; Tactile; Texture; Vibration; Vibrissa

Indexed keywords

DECISION MAKING; NEUROPHYSIOLOGY; NEUROSCIENCE; NONHUMAN; PERCEPTION; PRIORITY JOURNAL; PSYCHOPHYSICS; REVIEW; SENSORY RECEPTOR; SENSORY SYSTEM; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; TASK PERFORMANCE; VIBRISSA;

AFFERENT PATHWAYS; ANIMALS; RATS; SOMATOSENSORY CORTEX; TOUCH PERCEPTION; VIBRISSAE;

EID: 84875960522     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2012.05.013     Document Type: Review

References (96)

1. Adibi M., Arabzadeh E. A comparison of neuronal and behavioral detection and discrimination performances in rat whisker system. Journal of Neurophysiology 2011, 105:356-365.
2. Adibi M., Diamond M.E., Arabzadeh E. Behavioral study of whisker-mediated vibration sensation in rats. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:971-976.
3. Ahrens K.F., Kleinfeld D. Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. Journal of Neurophysiology 2004, 92:1700-1707.
4. Alloway K.D., Mutic J.J., Hoffer Z.S., Hoover J.E. Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex. Journal of Comparative Neurology 2000, 428:51-67.
5. Andres F.L., Van der Loos H. From sensory periphery to cortex: the architecture of the barrelfield as modified by various early manipulations of the mouse whiskerpad. Anatomy and Embryology 1985, 172:11-20.
6. Arabzadeh E., Panzeri S., Diamond M.E. Whisker vibration information carried by rat barrel cortex neurons. Journal of Neuroscience 2004, 24:6011-6020.
7. Arabzadeh E., Panzeri S., Diamond M.E. Deciphering the spike train of a sensory neuron: counts and temporal patterns in the rat whisker pathway. Journal of Neuroscience 2006, 26:9216-9226.
8. Arabzadeh E., Petersen R.S., Diamond M.E. Encoding of whisker vibration by rat barrel cortex neurons: implications for texture discrimination. Journal of Neuroscience 2003, 23:9146-9154.
9. Arabzadeh E., Zorzin E., Diamond M.E. Neuronal encoding of texture in the whisker sensory pathway. PLoS Biology 2005, 3:e17.
10. Berg R.W., Kleinfeld D. Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. Journal of Neurophysiology 2003, 89:104-117.
11. Birdwell J.A., Solomon J.H., Thajchayapong M., Taylor M.A., Cheely M., Towal R.B., Conradt J., Hartmann M.J. Biomechanical models for radial distance determination by the rat vibrissal system. Journal of Neurophysiology 2007, 98:2439-2455.
12. Brecht M., Preilowski B., Merzenich M.M. Functional architecture of the mystacial vibrissae. Behavioural Brain Research 1997, 84:81-97.
13. Burwell R.D., Amaral D.G. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Journal of Comparative Neurology 1998, 398:179-205.
14. Carvell G.E., Simons D.J. Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse. Somatosensory Research 1986, 3:213-237.
15. Carvell G.E., Simons D.J. Thalamic and corticocortical connections of the second somatic sensory area of the mouse. Journal of Comparative Neurology 1987, 265:409-427.
16. Carvell G.E., Simons D.J. Biometric analyses of vibrissal tactile discrimination in the rat. Journal of Neuroscience 1990, 10:2638-2648.
17. Carvell G.E., Simons D.J. Task- and subject-related differences in sensorimotor behavior during active touch. Somatosensory and Motor Research 1995, 12:1-9.
18. Chmielowska J., Carvell G.E., Simons D.J. Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. Journal of Comparative Neurology 1989, 285:325-338.
19. Clarke W., Bowsher D. Terminal distribution of primary afferent trigeminal fibers in the rat. Experimental Neurology 1962, 6:372-383.
20. Curtis J.C., Kleinfeld D. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nature Neuroscience 2009, 12:492-501.
21. Deschênes M., Timofeeva E., Lavallée P., Dufresne C. The vibrissal system as a model of thalamic operations. Progress in Brain Research 2005, 149:31-40.
22. Devlin J.T., Price C.J. Perirhinal contributions to human visual perception. Current Biology 2007, 17:1484-1488.
23. Diamond M.E. Texture sensation through the fingertips and the whiskers. Current Opinion in Neurobiology 2010, 20:319-327.
24. Diamond M.E., von Heimendahl M., Arabzadeh E. Whisker-mediated texture discrimination. PLoS Biology 2008, 6:e220.
25. Diamond M.E., von Heimendahl M., Itskov P., Arabzadeh E. Response to: Ritt et al., " embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats" . Neuron 2008, 57:599-613. Neuron 60, 743-744; author reply 745-747.
26. Diamond M.E., von Heimendahl M., Knutsen P.M., Kleinfeld D., Ahissar E. Where and what in the whisker sensorimotor system. Nature Reviews Neuroscience 2008, 9:601-612.
27. Dörfl J. The innervation of the mystacial region of the white mouse: a topographical study. Journal of Anatomy 1985, 142:173-184.
28. Ebara S., Kumamoto K., Matsuura T., Mazurkiewicz J.E., Rice F.L. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. Journal of Comparative Neurology 2002, 449:103-119.
29. Fassihi, A., Akrami, A., Esmaeili, V., Diamond, M.E., 2012. Sensation of a - noisy whisker vibration in rats: psychometric and neurometric analysis. Cosyne Abstracts 2012, Salt Lake City USA.
30. Fortin N.J., Wright S.P., Eichenbaum H. Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 2004, 431:188-191.
31. Gamzu E., Ahissar E. Importance of temporal cues for tactile spatial-frequency discrimination. Journal of Neuroscience 2001, 21:7416-7427.
32. Ganguly K., Kleinfeld D. Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sensory cortex in rat. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:12348-12353.
33. Gelbard-Sagiv H., Mukamel R., Harel M., Malach R., Fried I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 2008, 322:96-101.
34. Guic-Robles E., Jenkins W.M., Bravo H. Vibrissal roughness discrimination is barrelcortex-dependent. Behavioural Brain Research 1992, 48:145-152.
35. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
36. Harris J.A., Petersen R.S., Diamond M.E. Distribution of tactile learning and its neural basis. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:7587-7591.
37. Harvey M., Bermejo R., Zeigler H. Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. Somatosensory and Motor Research 2001, 18:211.
38. Hill D.N., Bermejo R., Zeigler H.P., Kleinfeld D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity. Journal of Neuroscience 2008, 28:3438-3455.
39. Hutson K.A., Masterton R.B. The sensory contribution of a single vibrissa's cortical barrel. Journal of Neurophysiology 1986, 56:1196-1223.
40. Itskov P.M., Vinnik E., Diamond M.E. Hippocampal representation of touch-guided behavior in rats: persistent and independent traces of stimulus and reward location. PLoS ONE 2011, 6:e16462.
41. Jadhav S.P., Wolfe J., Feldman D.E. Sparse temporal coding of elementary tactile features during active whisker sensation. Nature Neuroscience 2009, 12:792-800.
42. Jenks R.A., Vaziri A., Boloori A.R., Stanley G.B. Self-motion and the shaping of sensory signals. Journal of Neurophysiology 2010, 103:2195-2207.
43. Jones L.A., Lederman S.J. Human Hand Function 2006, Oxford University Press, USA.
44. Jones L.M., Lee S., Trageser J.C., Simons D.J., Keller A. Precise temporal responses in whisker trigeminal neurons. Journal of Neurophysiology 2004, 92:665-668.
45. Kepecs A., Uchida N., Zariwala H.A., Mainen Z.F. Neural correlates, computation and behavioural impact of decision confidence. Nature 2008, 455:227-231.
46. Kim U., Ebner F.F. Barrels and septa: separate circuits in rat barrels field cortex. Journal of Comparative Neurology 1999, 408:489-505.
47. Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Current Opinion in Neurobiology 2006, 16:435-444.
48. Knutsen P.M., Pietr M., Ahissar E. Haptic object localization in the vibrissal system: behavior and performance. Journal of Neuroscience 2006, 26:8451-8464.
49. Kouh M., Poggio T. A canonical neural circuit for cortical nonlinear operations. Neural Computation 2008, 20:1427-1451.
50. Kwegyir-Afful E.E., Keller A. Response properties of whisker-related neurons in rat second somatosensory cortex. Journal of Neurophysiology 2004, 92:2083-2092.
51. Lak A., Arabzadeh E., Diamond M.E. Enhanced response of neurons in rat somatosensory cortex to stimuli containing temporal noise. Cerebral Cortex 2008, 18:1085-1093.
52. Lak A., Arabzadeh E., Harris J., Diamond M. Correlated physiological and perceptual effects of noise in a tactile stimulus. Proceedings of the National Academy of Sciences of the United States of America 2010, 17:7981-7986.
53. Lavan D., McDonald J.S., Westbrook R.F., Arabzadeh E. Behavioural correlate of choice confidence in a discrete trial paradigm. PLoS ONE 2011, 6:e26863.
54. Lederman S.J., Klatzky R.L. Hand movements: a window into haptic object recognition. Cognitive Psychology 1987, 19:342-368.
55. Lichtenstein S.H., Carvell G.E., Simons D.J. Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosensory and Motor Research 1990, 7:47-65.
56. Lottem E., Azouz R. Dynamic translation of surface coarseness into whisker vibrations. Journal of Neurophysiology 2008, 100:2852.
57. Lottem E., Azouz R. A unifying framework underlying mechanotransduction in the somatosensory system. Journal of Neuroscience 2011, 31:8520-8532.
58. Maravall M., Petersen R.S., Fairhall A.L., Arabzadeh E., Diamond M.E. Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biology 2007, 5:e19.
59. Merleau-Ponty M. Phénoménologie de la perception 1945, Gallimard, Paris.
60. Mitchinson B., Arabzadeh E., Diamond M.E., Prescott T.J. Spike-timing in primary sensory neurons: a model of somatosensory transduction in the rat. Biological Cybernetics 2008, 98:185-194.
61. Mitchinson B., Gurney K.N., Redgrave P., Melhuish C., Pipe A.G., Pearson M., Gilhespy I., Prescott T.J. Empirically inspired simulated electro-mechanical model of the rat mystacial follicle-sinus complex. Proceedings of the Royal Society B: Biological Sciences 2004, 271:2509-2516.
62. Morita T., Kang H., Wolfe J., Jadhav S.P., Feldman D.E. Psychometric curve and behavioral strategies for whisker-based texture discrimination in rats. PLoS ONE 2011, 6:e20437.
63. Munk H. Ueber die Functionen der Grosshirnrinde; gesammelte Mittheilungen aus den Jahren 1877-80 1881, Hirschwald, Berlin.
64. Murphy R.A., Mondragon E., Murphy V.A. Rule learning by rats. Science 2008, 319:1849-1851.
65. Neff W.D., Diamond I.T. The neural basis of auditory discrimination. Biological and Biochemical Bases of Behavior 1958, 101-126. University of Wisconsin Press, Madison. H.F. Harlow, C.N. Woolsey (Eds.).
66. Nicholls J.G., Martin A.R., Fuchs P.A., Brown D.A., Diamond M.E., Weisblat D.A. From Neuron to Brain 2012, Sinauer, Sunderland, MA.
67. O'Keefe J. Place units in the hippocampus of the freely moving rat. Experimental Neurology 1976, 51:78-109.
68. Peretz I. The nature of music from a biological perspective. Cognition 2006, 100:1-32.
69. Perkon I., Kosir A., Itskov P.M., Tasic J.F., Diamond M.E. Unsupervised quantification of whisking and head movement in freely moving rodents. Journal of Neurophysiology 2011, 105:1950-1962.
70. Petersen R.S., Panzeri S., Maravall M. Neural coding and contextual influences in the whisker system. Biological Cybernetics 2009, 100:427-446.
71. Pons T.P., Garraghty P.E., Mishkin M. Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. Journal of Neurophysiology 1992, 68:518-527.
72. Prescott T.J., Diamond M.E., Wing A.M. Active touch sensing: an introduction to the theme issue. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2011, 366:2989-2995.
73. Rhodes D.H., Richmond M.E. Influence of soil texture, moisture and temperature on nest-site selection and burrowing by the pine vole, Microtus pinetorum. American Midland Naturalist 1985, 102-108.
74. Rice F.L., Mance A., Munger B.L. A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. Journal of Comparative Neurology 1986, 252:154-174.
75. Romo R., de Lafuente V. Conversion of sensory signals into perceptual decisions. Progress in Neurobiology 2012, in press. 10.1016/j.pneurobio.2012.03.007.
76. Shoykhet M., Doherty D., Simons D.J. Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing. Somatosensory and Motor Research 2000, 17:171-180.
77. Stuttgen M.C., Schwarz C. Psychophysical and neurometric detection performance under stimulus uncertainty. Nature Neuroscience 2008, 11:1091-1099.
78. Stüttgen M.C., Schwarz C. Integration of vibrotactile signals for whisker-related perception in rats Is governed by short time constants: comparison of neurometric and psychometric detection performance. Journal of Neuroscience 2010, 30:2060-2069.
79. Swanson L.W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Research 1981, 217:150-154.
80. Tafazoli S., Di Filippo A., Zoccolan D. Transformation-tolerant object recognition in rats revealed by visual priming. Journal of Neuroscience 2012, 32:21-34.
81. Thorpe S.J., Fize D., Marlot C. Speed of processing in the human visual system. Nature 1996, 381:520-522.
82. Torvik A. Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures; an experimental study in the rat. Journal of Comparative Neurology 1956, 106:51-141.
83. Veinante P., Deschenes M. Single-cell study of motor cortex projections to the barrel field in rats. Journal of Comparative Neurology 2003, 464:98-103.
84. Vincent S. The Functions of the Vibrissae in the Behavior of the White Rat 1912, University of Chicago.
85. Voges D., Carl K., Klauer G.J., Uhlig R., Schilling C., Behn C., Witte H. Structural characterisation of the whisker system of the rat. IEEE Sensors Journal 2012, 12:332-339.
86. von Heimendahl M., Itskov P.M., Arabzadeh E., Diamond M.E. Neuronal activity in rat barrel cortex underlying texture discrimination. PLoS Biology 2007, 5:e305.
87. Welker C., Woolsey T.A. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. Journal of Comparative Neurology 1974, 158:437-453.
88. Whitfield I.C. The object of the sensory cortex. Brain, Behavior and Evolution 1979, 16:129-154.
89. Williams C.M., Kramer E.M. The advantages of a tapered whisker. PLoS ONE 2010, 5:e8806.
90. Wolfe J., Hill D.N., Pahlavan S., Drew P.J., Kleinfeld D., Feldman D.E. Texture coding in the rat whisker system: slip-stick versus differential resonance. PloS Biology 2008, 6:e215.
91. Woolsey T.A., van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Research 1970, 17:205-242.
92. Wright A.K., Ramanathan S., Arbuthnott G.W. Identification of the source of the bilateral projection system from cortex to somatosensory neostriatum and an exploration of its physiological actions. Neuroscience 2001, 103:87-96.
93. Yamane Y., Carlson E.T., Bowman K.C., Wang Z., Connor C.E. A neural code for three-dimensional object shape in macaque inferotemporal cortex. Nature Neuroscience 2008, 11:1352-1360.
94. Yu C., Derdikman D., Haidarliu S., Ahissar E. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biology 2006, 4:e124.
95. Zoccolan D., Oertelt N., DiCarlo J.J., Cox D.D. A rodent model for the study of invariant visual object recognition. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:8748-8753.
96. Zuo Y., Perkon I., Diamond M.E. Whisking and whisker kinematics during a texture classification task. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2011, 366:3058-3069.