Neuronal basis for object location in the vibrissa scanning sensorimotor system

Neuron

Volumn 72, Issue 3, 2011, Pages 455-468

  Kleinfeld, David ^a   Deschênes, Martin ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; FUNCTIONAL ANATOMY; MOTOR CORTEX; NONHUMAN; OBJECT LOCATION; PERCEPTION; PRIORITY JOURNAL; REVIEW; RODENT; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; SENSORY CORTEX; VESTIBULAR SYSTEM; VIBRISSA;

AFFERENT PATHWAYS; ANIMALS; BRAIN MAPPING; HUMANS; NEURONS; NONLINEAR DYNAMICS; PERIODICITY; PHYSICAL STIMULATION; SOMATOSENSORY CORTEX; TOUCH; VIBRISSAE;

EID: 83455230840     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.10.009     Document Type: Review

References (140)

1. Ahissar E., Zacksenhouse M. Temporal and spatial coding in the rat vibrissal system. Prog. Brain Res. 2001, 130:75-87.
2. Ahissar E., Haidarliu S., Zacksenhouse M. Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. Proc. Natl. Acad. Sci. USA 1997, 94:11633-11638.
3. Alloway K.D. Information processing streams in rodent barrel cortex: the differential functions of barrel and septal circuits. Cereb. Cortex 2008, 18:979-989.
4. Alloway K.D., Smith J.B., Beauchemin K.J. Quantitative analysis of the bilateral brainstem projections from the whisker and forepaw regions in rat primary motor cortex. J. Comp. Neurol. 2010, 518:4546-4566.
5. Arenkiel B.R., Ehlers M.D. Molecular genetics and imaging technologies for circuit-based neuroanatomy. Nature 2009, 461:900-907.
6. Arenkiel B.R., Peca J., Davison I.G., Feliciano C., Deisseroth K., Augustine G.J., Ehlers M.D., Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 2007, 54:205-218.
7. Armstrong-James M., George M.J. Influence of anesthesia on spontaneous activity and receptive field size of single units in rat Sm1 neocortex. Exp. Neurol. 1988, 99:369-387.
8. Armstrong-James M., Fox K., Das-Gupta A. Flow of excitation within rat barrel cortex on striking a single vibrissa. J. Neurophysiol. 1992, 68:1345-1358.
9. Barthó P., Freund T.F., Acsády L. Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur. J. Neurosci. 2002, 16:999-1014.
10. Bautista D.M., Lumpkin E.A. Perspectives on: information and coding in mammalian sensory physiology: probing mammalian touch transduction. J. Gen. Physiol. 2011, 138:291-301.
11. Bellavance M.A., Demers M., Deschênes M. Feedforward inhibition determines the angular tuning of vibrissal responses in the principal trigeminal nucleus. J. Neurosci. 2010, 30:1057-1063.
12. Berg R.W., Kleinfeld D. Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J. Neurophysiol. 2003, 89:104-117.
13. Berg R.W., Friedman B., Schroeder L.F., Kleinfeld D. Activation of nucleus basalis facilitates cortical control of a brain stem motor program. J. Neurophysiol. 2005, 94:699-711.
14. Berryman L.J., Yau J.M., Hsiao S.S. Representation of object size in the somatosensory system. J. Neurophysiol. 2006, 96:27-39.
15. Bezdudnaya T., Castro-Alamancos M.A. Superior colliculus cells sensitive to active touch and texture during whisking. J. Neurophysiol. 2011, 106:332-346.
16. Bosman L.W.J., Koekkoek S.K., Shapiro J., Rijken B.F.M., Zandstra F., van der Ende B., Owens C.B., Potters J.W., de Gruijl J.R., Ruigrok T.J., De Zeeuw C.I. Encoding of whisker input by cerebellar Purkinje cells. J. Physiol. 2010, 588:3757-3783.
17. Bosman L.W.J., Houweling A.R., Owens C.B., Tanke N., Shevchouk O.T., Rahmati N., Teunissen W.H.T., Ju C., Gong W., Koekkoek S.K.E., et al. Anatomical pathways involved in generating and sensing rhythmic whisker movements. Front. Integr. Neurosci. 2011, Published online October 3, 2011. 10.3389/fnint.2011.00053.
18. Brecht M. Barrel cortex and whisker-mediated behaviors. Curr. Opin. Neurobiol. 2007, 17:408-416.
19. Brecht M., Preilowski B., Merzenich M.M. Functional architecture of the mystacial vibrissae. Behav. Brain Res. 1997, 84:81-97.
20. Brecht M., Krauss A., Muhammad S., Sinai-Esfahani L., Bellanca S., Margrie T.W. Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J. Comp. Neurol. 2004, 479:360-373.
21. Brecht M., Schneider M., Sakmann B., Margrie T.W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 2004, 427:704-710.
22. Brown A.W.S., Waite P.M.E. Responses in the rat thalamus to whisker movements produced by motor nerve stimulation. J. Physiol. 1974, 238:387-401.
23. Bureau I., von Saint Paul F., Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 2006, 4:e382. 10.1371/journal.pbio.0040382.
24. Carvell G.E., Simons D.J. Task- and subject-related differences in sensorimotor behavior during active touch. Somatosens. Mot. Res. 1995, 12:1-9.
25. Carvell G.E., Miller S.A., Simons D.J. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens. Mot. Res. 1996, 13:115-127.
26. Castro-Alamancos M.A. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog. Neurobiol. 2004, 74:213-247.
27. Cohen J.D., Castro-Alamancos M.A. Behavioral state dependency of neural activity and sensory (whisker) responses in superior colliculus. J. Neurophysiol. 2010, 104:1661-1672.
28. Crochet S., Petersen C.C.H. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 2006, 9:608-610.
29. Cullen K.E., Brooks J.X., Jamali M., Carriot J., Massot C. Internal models of self-motion: computations that suppress vestibular reafference in early vestibular processing. Exp. Brain Res. 2011, 210:377-388.
30. Curtis J.C., Kleinfeld D. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nat. Neurosci. 2009, 12:492-501.
31. de Kock C.P., Sakmann B. Spiking in primary somatosensory cortex during natural whisking in awake head-restrained rats is cell-type specific. Proc. Natl. Acad. Sci. USA 2009, 106:16446-16450.
32. Descartes, R. (1637). Discourse on Methods, Optics, Geometry, and Meteorology, P.J. Olscamp (trans.) (Indianapolis, IN: Hackett Publsihing Compant).
33. Deschênes M., Timofeeva E., Lavallée P., Dufresne C. The vibrissal system as a model of thalamic operations. Prog. Brain Res. 2005, 149:31-40.
34. Diamond M.E., Armstrong-James M., Budway M.J., Ebner F.F. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J. Comp. Neurol. 1992, 319:66-84.
35. Diamond M.E., von Heimendahl M., Knutsen P.M., Kleinfeld D., Ahissar E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 2008, 9:601-612.
36. Dombeck D.A., Khabbaz A.N., Collman F., Adelman T.L., Tank D.W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 2007, 56:43-57.
37. Erzurumlu R.S., Killackey H.P. Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat. J. Comp. Neurol. 1979, 188:75-86.
38. Fairhall A.L., Lewen G.D., Bialek W., de Ruyter Van Steveninck R.R. Efficiency and ambiguity in an adaptive neural code. Nature 2001, 412:787-792.
39. Fee M.S., Mitra P.P., Kleinfeld D. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J. Neurophysiol. 1997, 78:1144-1149.
40. Fox K. Barrel Cortex 2008, Cambridge University Press, Cambridge.
41. Friedman W.A., Zeigler H.P., Keller A. Vibrissae motor cortex unit activity during whisking. J. Neurophysiol. 2011, in press. Published online October 12, 2011. 10.1152/jn.00659.2011.
42. Furuta T., Timofeeva E., Nakamura K., Okamoto-Furuta K., Togo M., Kaneko T., Deschênes M. Inhibitory gating of vibrissal inputs in the brainstem. J. Neurosci. 2008, 28:1789-1797.
43. Ganguly K., Kleinfeld D. Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sensory cortex in rat. Proc. Natl. Acad. Sci. USA 2004, 101:12348-12353.
44. Gao P., Bermejo R., Zeigler H.P. Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J. Neurosci. 2001, 21:5374-5380.
45. Gentet L.J., Avermann M., Matyas F., Staiger J.F., Petersen C.C.H. Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 2010, 65:422-435.
46. Gibson J.J. Observations on active touch. Psychol. Rev. 1962, 69:477-491.
47. Gradinaru V., Thompson K.R., Zhang F., Mogri M., Kay K., Schneider M.B., Deisseroth K. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 2007, 27:14231-14238.
48. Green A.M., Angelaki D.E. Internal models and neural computation in the vestibular system. Exp. Brain Res. 2010, 200:197-222.
49. Grinevich V., Brecht M., Osten P. Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J. Neurosci. 2005, 25:8250-8258.
50. Gustafson J.W., Felbain-Keramidas S.L. Behavioral and neural approaches to the function of the mystacial vibrissae. Psychol. Bull. 1977, 84:477-488.
51. Haidarliu S., Ahissar E. Size gradients of barreloids in the rat thalamus. J. Comp. Neurol. 2001, 429:372-387.
52. Haidarliu S., Yu C., Rubin N., Ahissar E. Lemniscal and extralemniscal compartments in the VPM of the rat. Front. Neuroanat. 2008, 2:4.
53. Haidarliu S., Simony E., Golomb D., Ahissar E. Muscle architecture in the mystacial pad of the rat. Anat. Rec. (Hoboken) 2010, 293:1192-1206.
54. Hartmann M.J. A night in the life of a rat: vibrissal mechanics and tactile exploration. Ann. N Y Acad. Sci. 2011, 1225:110-118.
55. Hattox A.M., Priest C.A., Keller A. Functional circuitry involved in the regulation of whisker movements. J. Comp. Neurol. 2002, 442:266-276.
56. Harvey M.A., Bermejo R., Zeigler H.P. Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. Somatosens. Mot. Res. 2001, 18:211-222.
57. Hasegawa H., Abbott S., Han B.-X., Qi Y., Wang F. Analyzing somatosensory axon projections with the sensory neuron-specific Advillin gene. J. Neurosci. 2007, 27:14404-14414.
58. Hemelt M.E., Keller A. Superior colliculus control of vibrissa movements. J. Neurophysiol. 2008, 100:1245-1254.
59. 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. J. Neurosci. 2008, 28:3438-3455.
60. Hill D.N., Curtis J.C., Moore J.D., Kleinfeld D. Primary motor cortex reports efferent control of vibrissa position on multiple time scales. Neuron 2011, 72:344-356.
61. Hill D.N., Mehta S.B., Kleinfeld D. Quality metrics to accompany spike sorting of extracellular signals. J. Neurosci. 2011, 31:8699-8705.
62. Hippenmeyer S., Vrieseling E., Sigrist M., Portmann T., Laengle C., Ladle D.R., Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 2005, 3:e159. 10.1371/journal.pbio.0030159.
63. Hoffer Z.S., Hoover J.E., Alloway K.D. Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row. J. Comp. Neurol. 2003, 466:525-544.
64. Hoffer Z.S., Arantes H.B., Roth R.L., Alloway K.D. Functional circuits mediating sensorimotor integration: quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons. J. Comp. Neurol. 2005, 488:82-100.
65. Hutson K.A., Masterton R.B. The sensory contribution of a single vibrissa's cortical barrel. J. Neurophysiol. 1986, 56:1196-1223.
66. Jones E.G., Diamond I.T. Cerebral Cortex: The Barrel Cortex of Rodents 1995, Volume 11. Springer, New York.
67. Khatri V., Hartings J.A., Simons D.J. Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. J. Neurophysiol. 2004, 92:3244-3254.
68. Khatri V., Bermejo R., Brumberg J.C., Keller A., Zeigler H.P. Whisking in air: Encoding of kinetmatics by trigeminal ganglion neurons in awake rats. J. Neurophysiol. 2009, 101:836-886.
69. Khatri V., Bermejo R., Brumberg J.C., Zeigler H.P. Whisking in air: encoding of kinematics by VPM neurons in awake rats. Somatosens. Mot. Res. 2010, 27:111-120.
70. Killackey H.P., Erzurumlu R.S. Trigeminal projections to the superior colliculus of the rat. J. Comp. Neurol. 1981, 201:221-242.
71. Kim J.N., Koh K.S., Lee E., Park S.C., Song W.C. The morphology of the rat vibrissal follicle-sinus complex revealed by three-dimensional computer-aided reconstruction. Cells Tissues Organs 2011, 193:207-214.
72. Klein B.G., Rhoades R.W. Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J. Comp. Neurol. 1985, 232:55-69.
73. Kleinfeld D., Berg R.W., O'Connor S.M. Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens. Mot. Res. 1999, 16:69-88.
74. Kleinfeld D., Sachdev R.N.S., Merchant L.M., Jarvis M.R., Ebner F.F. Adaptive filtering of vibrissa input in motor cortex of rat. Neuron 2002, 34:1021-1034.
75. Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 2006, 16:435-444.
76. Knutsen P.M., Ahissar E. Orthogonal coding of object location. Trends Neurosci. 2009, 32:101-109.
77. Knutsen P.M., Pietr M., Ahissar E. Haptic object localization in the vibrissal system: behavior and performance. J. Neurosci. 2006, 26:8451-8464.
78. König P., Luksch H. Active sensing-closing multiple loops. Z. Naturforsch., C, J. Biosci. 1998, 53:542-549.
79. Krupa D.J., Matell M.S., Brisben A.J., Oliveira L.M., Nicolelis M.A.L. Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J. Neurosci. 2001, 21:5752-5763.
80. Kublik E. Contextual impact on sensory processing at the barrel cortex of awake rat. Acta Neurobiol. Exp. (Warsz.) 2004, 64:229-238.
81. Lang E.J., Sugihara I., Llinás R. Olivocerebellar modulation of motor cortex ability to generate vibrissal movements in rat. J. Physiol. 2006, 571:101-120.
82. Lee A.K., Manns I.D., Sakmann B., Brecht M. Whole-cell recordings in freely moving rats. Neuron 2006, 51:399-407.
83. Leiser S.C., Moxon K.A. Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat. Neuron 2007, 53:117-133.
84. London M., Häusser M. Dendritic computation. Annu. Rev. Neurosci. 2005, 28:503-532.
85. Lübke J., Feldmeyer D. Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct. Funct. 2007, 212:3-17.
86. Lundstrom B.N., Famulare M., Sorensen L.B., Spain W.J., Fairhall A.L. Sensitivity of firing rate to input fluctuations depends on time scale separation between fast and slow variables in single neurons. J. Comput. Neurosci. 2009, 27:277-290.
87. Luo W., Enomoto H., Rice F.L., Milbrandt J., Ginty D.D. Molecular identification of rapidly adapting mechanoreceptors and their developmental dependence on ret signaling. Neuron 2009, 64:841-856.
88. Mao T., Kusefoglu D., Hooks B.M., Huber D., Petreanu L., Svoboda K. Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 2011, 72:111-123.
89. Masri R., Bezdudnaya T., Trageser J.C., Keller A. Encoding of stimulus frequency and sensor motion in the posterior medial thalamic nucleus. J. Neurophysiol. 2008, 100:681-689.
90. Matyas F., Sreenivasan V., Marbach F., Wacongne C., Barsy B., Mateo C., Aronoff R., Petersen C.C. Motor control by sensory cortex. Science 2010, 330:1240-1243.
91. Mehta S.B., Whitmer D., Figueroa R., Williams B.A., Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 2007, 5:e15. 10.1371/journal.pbio.0050015.
92. Meyer H.S., Wimmer V.C., Hemberger M., Bruno R.M., de Kock C.P., Frick A., Sakmann B., Helmstaedter M. Cell type-specific thalamic innervation in a column of rat vibrissal cortex. Cereb. Cortex 2010, 20:2287-2303.
93. Mitchinson B., Martin C.J., Grant R.A., Prescott T.J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 2007, 274:1035-1041.
94. Mitchinson B., Grant R.A., Arkley K., Rankov V., Perkon I., Prescott T.J. Active vibrissal sensing in rodents and marsupials. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:3037-3048.
95. Mittmann W., Wallace D.J., Czubayko U., Herb J.T., Schaefer A.T., Looger L.L., Denk W., Kerr J.N. Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat. Neurosci. 2011, 14:1089-1093.
96. Miyashita E., Keller A., Asanuma H. Input-output organization of the rat vibrissal motor cortex. Exp. Brain Res. 1994, 99:223-232.
97. Moore C.I., Nelson S.B., Sur M. Dynamics of neuronal processing in rat somatosensory cortex. Trends Neurosci. 1999, 22:513-520.
98. Mosconi T.M., Rice F.L., Song M.J. Sensory innervation in the inner conical body of the vibrissal follicle-sinus complex of the rat. J. Comp. Neurol. 1993, 328:232-251.
99. Nakamura S., Narumi T., Tsutsui K.-I., Iijima T. Difference in the functional significance between the lemniscal and paralemniscal pathways in the perception of direction of single whisker stimulation examined by muscimol microinjection. Neurosci. Res. 2009, 64:323-329.
100. Nelson M.E., MacIver M.A. Sensory acquisition in active sensing systems. J. Comp. Physiol. Sensory Neural. Behav. Physiol. 2006, 192:573-586.
101. Nguyen Q.-T., Kleinfeld D. Positive feedback in a brainstem tactile sensorimotor loop. Neuron 2005, 45:447-457.
102. Nguyen Q.-T., Wessel R., Kleinfeld D. Developmental regulation of active and passive membrane properties in rat vibrissa motoneurones. J. Physiol. 2004, 556:203-219.
103. O'Connor D.H., Huber D., Svoboda K. Reverse engineering the mouse brain. Nature 2009, 461:923-929.
104. O'Connor D.H., Clack N.G., Huber D., Komiyama T., Myers E.W., Svoboda K. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 2010, 30:1947-1967.
105. O'Connor D.H., Peron S.P., Huber D., Svoboda K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 2010, 67:1048-1061.
106. Perkon I., Kosir A., Itskov P.M., Tasic J., Diamond M.E. Unsupervised quantification of whisking and head movement in freely moving rodents. J. Neurophysiol. 2011, 105:1950-1962.
107. Petersen C.C. The functional organization of the barrel cortex. Neuron 2007, 56:339-355.
108. Petersen R.S., Panzeri S., Diamond M.E. Population coding in somatosensory cortex. Curr. Opin. Neurobiol. 2002, 12:441-447.
109. Pidoux M., Mahon S., Deniau J.-M., Charpier S. Integration and propagation of somatosensory responses in the corticostriatal pathway: an intracellular study in vivo. J. Physiol. 2011, 589:263-281.
110. Pierret T., Lavallée P., Deschênes M. Parallel streams for the relay of vibrissal information through thalamic barreloids. J. Neurosci. 2000, 20:7455-7462.
111. Pietr M.D., Knutsen P.M., Shore D.I., Ahissar E., Vogel Z. Cannabinoids reveal separate controls for whisking amplitude and timing in rats. J. Neurophysiol. 2010, 104:2532-2542.
112. Polley D.B., Rickert J.L., Frostig R.D. Whisker-based discrimination of object orientation determined with a rapid training paradigm. Neurobiol. Learn. Mem. 2005, 83:134-142.
113. Rice F.L. Structure, vascularization, and innervation of the mystacial pad of the rat as revealed by the lectin Griffonia simplicifolia. J. Comp. Neurol. 1993, 337:386-399.
114. Richmond B.J., Wurtz R.H. Vision during saccadic eye movements. II. A corollary discharge to monkey superior colliculus. J. Neurophysiol. 1980, 43:1156-1167.
115. Sachdev R.N.S., Berg R.W., Champney G., Kleinfeld D., Ebner F.F. Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking. Somatosens. Mot. Res. 2003, 20:163-169.
116. Sato T.R., Svoboda K. The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 2010, 30:4256-4260.
117. Sawinski J., Wallace D.J., Greenberg D.S., Grossmann S., Denk W., Kerr J.N.D. Visually evoked activity in cortical cells imaged in freely moving animals. Proc. Natl. Acad. Sci. USA 2009, 106:19557-19562.
118. Schubert D., Kötter R., Staiger J.F. Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 2007, 212:107-119.
119. Seung H.S., Sompolinsky H. Simple models for reading neuronal population codes. Proc. Natl. Acad. Sci. USA 1993, 90:10749-10753.
120. Shortland P.J., DeMaro J.A., Jacquin M.F. Trigeminal structure-function relationships: a reevaluation based on long-range staining of a large sample of brainstem a beta fibers. Somatosens. Mot. Res. 1995, 12:249-275.
121. Shortland P.J., Demaro J.A., Shang F., Waite P.M.E., Jacquin M.F. Peripheral and central predictors of whisker afferent morphology in the rat brainstem. J. Comp. Neurol. 1996, 375:481-501.
122. Shuler M.G., Krupa D.J., Nicolelis M.A. Bilateral integration of whisker information in the primary somatosensory cortex of rats. J. Neurosci. 2001, 21:5251-5261.
123. Simons D.J. Response properties of vibrissa units in rat SI somatosensory neocortex. J. Neurophysiol. 1978, 41:798-820.
124. Simons D.J., Carvell G.E. Thalamocortical response transformation in the rat vibrissa/barrel system. J. Neurophysiol. 1989, 61:311-330.
125. Solomon J.H., Hartmann M.J. Biomechanics: robotic whiskers used to sense features. Nature 2006, 443:525.
126. Sommer M.A., Wurtz R.H. A pathway in primate brain for internal monitoring of movements. Science 2002, 296:1480-1482.
127. Swadlow H.A. Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2002, 357:1717-1727.
128. Szwed M., Bagdasarian K., Ahissar E. Encoding of vibrissal active touch. Neuron 2003, 40:621-630.
129. Towal R.B., Hartmann M.J. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J. Neurosci. 2006, 26:8838-8846.
130. Travers J.B. Oromotor nuclei. The Rat Nervous System 1995, 239-255. Academic Press, San Diego, CA. Second Edition. G. Paxinos (Ed.).
131. Urbain N., Deschênes M. Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron 2007, 56:714-725.
132. Urbain N., Deschênes M. A new thalamic pathway of vibrissal information modulated by the motor cortex. J. Neurosci. 2007, 27:12407-12412.
133. Veinante P., Jacquin M.F., Deschênes M. Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat. J. Comp. Neurol. 2000, 420:233-243.
134. Vincent S.B. The function of the vibrissae in the behavior of the white rat. Behavior Monographs 1912, 1:7-81.
135. Wachowiak M. All in a sniff: olfaction as a model for active sensing. Neuron 2011, 71:962-973.
136. Welker W.I. Analysis of sniffing of the albino rat. Behaviour 1964, 12:223-244.
137. Wise S.P., Jones E.G. Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J. Comp. Neurol. 1977, 175:129-157.
138. Wurtz R.H., McAlonan K., Cavanaugh J., Berman R.A. Thalamic pathways for active vision. Trends Cogn. Sci. (Regul. Ed.) 2011, 15:177-184.
139. Yu C., Derdikman D., Haidarliu S., Ahissar E. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 2006, 4:e124. 10.1371/journal.pbio.0040124.
140. Zucker E., Welker W.I. Coding of somatic sensory input by vibrissae neurons in the rat's trigeminal ganglion. Brain Res. 1969, 12:138-156.