Somatotopic direct projections from orofacial areas of secondary somatosensory cortex to trigeminal sensory nuclear complex in rats

Neuroscience

Volumn 219, Issue , 2012, Pages 214-233

  Haque, T ^a   Akhter, F ^a   Kato, T ^a   Sato, F ^a   Takeda, R ^a   Higashiyama, K ^a   Moritani, M ^b   Bae, Y C ^c   Sessle, B J ^d   Yoshida, A ^a  

^a OSAKA UNIVERSITY   (Japan)

^b MORINOMIYA UNIVERSITY OF MEDICAL SCIENCES   (Japan)

^c Kyungpook National University   (South Korea)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Corticofugal; Feedback; S1; S2; SII

Indexed keywords

BIOTINYLATED DEXTRANAMINE; FLUOROGOLD; TRACER; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CORTEX; BRAIN REGION; CELL LABELING; FACE; MEDULLA OBLONGATA; MORPHOLOGY; NERVE CELL; NERVE ENDING; NERVE PROJECTION; NERVE STIMULATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PONS; PRINCIPAL SENSORY NUCLEUS; PRIORITY JOURNAL; RAT; SECONDARY SOMATOSENSORY CORTEX; SENSORY NERVE; SOMATOSENSORY SYSTEM; TRIGEMINAL NERVE;

ANIMALS; FACE; MALE; NEURAL PATHWAYS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; TRIGEMINAL NUCLEI;

EID: 84863998536     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.05.065     Document Type: Article

References (118)

1. Adams J.C. Technical considerations on the use of HRP as a neuronal marker. Neuroscience 1977, 2:141-145.
2. Alloway K.D., Hoffer Z.S., Hoover J.E. Quantitative comparisons of corticothalamic topography within the ventrobasal complex and the posterior nucleus of the rodent thalamus. Brain Res 2003, 968:54-68.
3. 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. J Comp Neurol 2000, 426:51-67.
4. Arvidsson J. Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 1982, 211:84-92.
5. Benison A.M., Rector D.M., Barth D.S. Hemispheric mapping of secondary somatosensory cortex in the rat. J Neurophysiol 2007, 97:200-207.
6. Bereiter D.A., Bereiter D.F., Ramos M. Vagotomy prevents morphine-induced reduction in Fos-like immunoreactivity in trigeminal spinal nucleus produced after TMJ injury in a sex-dependent manner. Pain 2002, 96:205-213.
7. Brett-Green B., Paulsen M., Staba R.J., Fifkova E., Barth D.S. Two distinct regions of secondary somatosensory cortex in the rat: topographical organization and multisensory responses. J Neurophysiol 2004, 91:1327-1336.
8. Brodal A., Szabo T., Torvik A. Corticofugal fibers to sensory trigeminal nuclei and nucleus of solitary tract. An experimental study in the cat. J Comp Neurol 1956, 106:527-556.
9. Bruce L.L., McHaffie J.G., Stein B.E. The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J Comp Neurol 1987, 262:315-330.
10. Carvell G.E., Simons D.J. Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse. Somatosens Res 1986, 3:213-237.
11. Carvell G.E., Simons D.J. Thalamic and corticocortical connections of the second somatic sensory area of the mouse. J Comp Neurol 1987, 265:409-427.
12. Caselli R. Ventrolateral and dorsomedial somatosensory association cortex damage produces distinct somesthetic syndromes in humans. Neurology 1993, 43:762-771.
13. Chang Z., Haque T., Iida C., Seki S., Sato F., Kato T., Uchino K., Ono T., Nakamura M., Bae Y.-C., Yoshida A. Distribution of premotoneurons for jaw-closing and jaw-opening motor nucleus receiving contacts from axon terminals of primary somatosensory cortical neurons in rats. Brain Res 2009, 1275:43-53.
14. Chiaia N.L., Hess P.R., Hosoi M., Rhoades R.W. Morphological characteristics of low-threshold primary afferents in the trigeminal subnuclei interpolaris and caudalis (the medullary dorsal horn) of the golden hamster. J Comp Neurol 1987, 264:527-546.
15. Chiaia N.L., Rhoades R.W., Bennett-Clarke C.A., Fish S.E., Killackey H.P. Thalamic processing of vibrissal information in the rat. I. Afferent input to the medial ventral posterior and posterior nuclei. J Comp Neurol 1991, 314:201-216.
16. Darian-Smith I., Yokota T. Cortically evoked depolarization of trigeminal cutaneous afferent fibers in the cat. J Neurophysiol 1966, 29:170-184.
17. Déjerine J. Sémiologie des affections du syste me neveux 1914, Masson, Paris.
18. Desbois C., Le Bars D., Villanueva L. Organization of cortical projections to the medullary subnucleus reticularis dorsalis: a retrograde and anterograde tracing study in the rat. J Comp Neurol 1999, 410:178-196.
19. Dessem D., Luo P. Jaw-muscle spindle afferent feedback to the cervical spinal cord in the rat. Exp Brain Res 1999, 128:451-459.
20. Donoghue J.P., Wenthold R.J., Altschuler R.A. Localization of glutaminase-like and aspartate aminotransferase-like immunoreactivity in neurons of cerebral neocortex. J Neurosci 1985, 5:2597-2608.
21. Dubner R. Interaction of peripheral and central input in the main sensory trigeminal nucleus of the cat. Exp Neurol 1967, 17:186-202.
22. Dubner R., Sessle B.J. Presynaptic excitability changes of primary afferent and corticofugal fibers projecting to trigeminal brain stem nuclei. Exp Neurol 1971, 30:223-238.
23. Dunn R.C., Chong K.L. Sensorimotor cortical projections to the marginal zone of the trigeminal subnucleus caudalis. Brain Res 1982, 232:171-176.
24. Dunn R.C., Tolbert D.L. The corticotrigeminal projection in the cat. A study of the organization of cortical projections to the spinal trigeminal nucleus. Brain Res 1982, 240:13-25.
25. Erzurumlu R.S., Killackey H.P. Diencephalic projections of the subnucleus interpolaris of the brainstem trigeminal complex in the rat. Neuroscience 1980, 5:1891-1901.
26. Fabri M., Burton H. Ipsilateral cortical connections of primary somatic sensory cortex in rats. J Comp Neurol 1991, 311:405-424.
27. Fukushima T., Kerr F.W.L. Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol 1979, 183:169-184.
28. Furuta T., Urbain N., Kaneko T., Deschênes M. Corticofugal control of vibrissa-sensitive neurons in the interpolaris nucleus of the trigeminal complex. J Neurosci 2010, 30:1832-1838.
29. Garcha H.S., Ettlinger G. The effects of unilateral or bilateral removals of the second somatosensory cortex (SII): a profound tactile disorder in monkeys. Cortex 1978, 14:319-326.
30. Giuffrida R., Rustioni A. Glutamate and aspartate immunoreactivity in corticospinal neurons of rats. J Comp Neurol 1989, 288:154-164.
31. Gobel S. Structural organization in the main sensory trigeminal nucleus. Oral-facial sensory and motor mechanisms 1971, 183-203. Appleton-Century-Crofts, New York. R. Dubner, Y. Kawamura (Eds.).
32. Greenwood L.F., Sessle B.J. Inputs to trigeminal brain stem neurones from facial, oral, tooth pulp and pharyngolaryngeal tissues: II. Role of trigeminal nucleus caudalis in modulating responses to innocuous and noxious stimuli. Brain Res 1976, 117:227-238.
33. Hayashi H. Differential terminal distribution of single large cutaneous afferent fibers in the spinal trigeminal nucleus and in the cervical spinal dorsal horn. Brain Res 1982, 244:173-177.
34. Hayashi H. Morphology of central terminations of intra-axonally stained large myelinated primary afferent fibers from facial skin in the rat. J Comp Neurol 1985, 237:195-215.
35. Hernández-Peón R., Hagbarth K.E. Interaction between afferent and cortically induced reticular responses. J Neurophysiol 1955, 18:44-55.
36. Hu J.W., Dostrovsky J.O., Sessle B.J. Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). I. Responses to oral-facial noxious and nonnoxious stimuli and projections to thalamus and subnucleus oralis. J Neurophysiol 1981, 45:173-192.
37. Inoue M., Nozawa-Inoue K., Donga R., Yamada Y. Convergence of selected inputs from sensory afferents to trigeminal premotor neurons with possible projections to masseter motoneurons in the rabbit. Brain Res 2002, 957:183-191.
38. Inui K., Wang X., Tamura Y., Kaneoke Y., Kakigi R. Serial processing in the human somatosensory system. Cerebral Cortex 2004, 14:851-857.
39. Jacquin M.F., Barcia M., Rhoades R.W. Structure-function relationships in rat brainstem subnucleus interpolaris: IV. Projection neurons. J Comp Neurol 1989, 282:45-62.
40. Jacquin M.F., Chiaia N.L., Rhoades R.W. Trigeminal projections to contralateral dorsal horn: central extent, peripheral origins, and plasticity. Somatosens Mot Res 1990, 7:153-183.
41. Jacquin M.F., Mooney R.D., Rhoades R.W. Morphology, response properties, and collateral projections of trigeminothalamic neurons in brainstem subnucleus interpolaris of rat. Exp Brain Res 1986, 61:457-468.
42. Jacquin M.F., Renehan W.E., Mooney R.D., Rhoades R.W. Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 1986, 55:1153-1186.
43. Jacquin M.F., Rhoades R.W. Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Mot Res 1990, 7:265-288.
44. Jacquin M.F., Semba K., Rhoades R.W., Egger M.D. Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei. Brain Res 1982, 246:285-291.
45. Jacquin M.F., Wiegand M.R., Renehan W.E. Structure-functional relationships in rat brain stem subnucleus interpolaris. VIII. Cortical inputs. J Neurophysiol 1990, 64:3-27.
46. Jones B.E., Yang T.Z. The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 1985, 242:56-92.
47. Kawana E. Projections of the anterior ectosylvian gyrus to the thalamus, the dorsal column nuclei, the trigeminal nuclei and the spinal cord in cats. Brain Res 1969, 14:117-136.
48. Kemplay S., Webster K.E. A quantitative study of the projections of the gracile, cuneate and trigeminal nuclei and of the medullary reticular formation to the thalamus in the rat. Neuroscience 1989, 32:153-167.
49. Killackey H.P., Koralek K.A., Chiaia N.L., Rhodes R.W. Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex. J Comp Neurol 1989, 282:428-445.
50. Kriegsfeld L.J., Leak R.K., Yackulic C.B., LeSauter J., Silver R. Organization of suprachiasmatic nucleus projections in Syrian hamsters (mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 2004, 468:361-379.
51. Krnjevic K., Phillis J.W. Actions of certain amines on cerebral cortical neurons. Br J Pharmacol Chemother 1963, 20:471-490.
52. Kuypers H.G. Central cortical projections to motor and somatosensory cell groups. An experimental study in the rhesus monkey. Brain 1960, 83:161-184.
53. Leak R.K., Moore R.Y. Identification of retinal ganglion cells projecting to the lateral hypothalamic area of the rat. Brain Res 1997, 770:105-114.
54. Leak R.K., Moore R.Y. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 2001, 433:312-334.
55. Luo P., Dessem D. Inputs from identified jaw-muscle spindle afferents to trigeminothalamic neurons in the rat: a double-labeling study using retrograde HRP and intracellular biotinamide. J Comp Neurol 1995, 353:50-66.
56. Luo P., Moritani M., Dessem D. Jaw-muscle spindle afferent pathways to the trigeminal motor nucleus in the rat. J Comp Neurol 2001, 435:341-353.
57. Marfurt C.F., Rajchert D.M. Trigeminal primary afferent projections to " nontrigeminal" areas of the rat central nervous system. J Comp Neurol 1991, 303:489-511.
58. Matano S., Shigenaga Y., Hiura T., Sakai A. The cortico-thalamic and -bulbar projections from the somatic sensory face area in the rat. Okajima Fol Anat Jap 1972, 49:249-270.
59. Menzel R., Barth D.S. Multisensory and secondary somatosensory cortex in the rat. Cerebral Cortex 2005, 15:1690-1696.
60. Mettler F.A. Corticofugal fiber connections of the cortex of the Macaca mulatta. The frontal region. J Comp Neurol 1935, 61:509-542.
61. Mettler F.A. Corticofugal fiber connections of the cortex of the Macaca mulatta. The parietal region. J Comp Neurol 1935, 62:263-291.
62. Mima T., Nagamine T., Nakamura K., Shibasaki H. Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. J Neurophysiol 1998, 80:2215-2221.
63. Moga M.M., Saper C.B. Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J Comp Neurol 1994, 346:137-150.
64. Nakata H., Inui K., Wasaka T., Tamura Y., Tran T.D., Qiu Y., Wang X., Nguyen T.B., Kakigi R. Movements modulate cortical activities evoked by noxious stimulation. Pain 2004, 107:91-98.
65. Nasution I.D., Shigenaga Y. Ascending and descending internuclear projections within the trigeminal sensory nuclear complex. Brain Res 1987, 425:234-247.
66. Nishiike S., Guldin W.O., Bäurle J. Corticofugal connections between the cerebral cortex and the vestibular nuclei in the rat. J Comp Neurol 2000, 420:363-372.
67. Nishimori T., Sera M., Suemune S., Yoshida A., Tsuru K., Tsuiki Y., Akisaka T., Okamoto T., Dateoka Y., Shigenaga Y. The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei. Brain Res 1986, 372:375-381.
68. Nord S.G. Somatotopic organization in the spinal trigeminal nucleus, the dorsal column nuclei and related structures in the rat. J Comp Neurol 1967, 130:343-356.
69. Nuñez A., Malmierca E. Corticofugal modulation of sensory information. Adv Anat Embryol Cell Biol 2007, 187:1-74.
70. Olsson K.å., Landgren S., Westberg K.G. Location of, and peripheral convergence on, the interneuron in the disynaptic path from the coronal gyrus of the cerebral cortex to the trigeminal motoneurons in the cat. Exp Brain Res 1986, 65:83-97.
71. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Sydney. 2nd ed.
72. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Sydney. 4th ed.
73. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, Sydney. 6th ed.
74. Pierret T., Lavallée P., Deschênes M. Parallel streams for the relay of vibrissal information through thalamic barreloids. J Neurosci 2000, 20:7455-7462.
75. Price D.D., Dubner R., Hu J.W. Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J Neurophysiol 1976, 39:936-953.
76. Remple M.S., Henry E.C., Catania K.C. Organization of somatosensory cortex in the laboratory rat (Rattus norvegicus): evidence for two lateral areas joined at the representation of the teeth. J Comp Neurol 2003, 467:105-118.
77. Renehan W.E., Jacquin M.F. Anatomy of central nervous system pathways related to head pain. The headaches 1993, 59-68. Raven Press, New York. J. Olesen, P. Tfelt-Hansen, K.M.A. Welch (Eds.).
78. Ridley R.M., Ettlinger G. Impaired tactile learning and retention after removals of the second somatic projection cortex (SII) in the monkey. Brain Res 1976, 109:656-660.
79. Ridley R.M., Ettlinger G. Further evidence of impaired tactile learning after removals of the second somatic sensory projection cortex (SII) in the monkey. Exp Brain Res 1978, 31:475-488.
80. Romo R., Hernández A., Zainos A., Lemus L., Brody C.D. Neural correlates of decision-making in secondary somatosensory cortex. Nat Neurosci 2002, 5:1217-1225.
81. Sessle B.J., Hu J.W., Dubner R., Lucier G.E. Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). II. Modulation of responses to noxious and nonnoxious stimuli by periaqueductal gray, nucleus raphe magnus, cerebral cortex, and afferent influences, and effect of naloxone. J Neurophysiol 1981, 45:193-207.
82. Shi C.-J., Cassell M.D. Cortical, thalamic, and amygdaloid projections of rat temporal cortex. J Comp Neurol 1997, 382:153-175.
83. Shigenaga Y., Chen I.C., Suemune S., Nishimori T., Nasution I.D., Yoshida A., Sato H., Okamoto T., Sera M., Hosoi M. Oral and facial representation within the medullary and upper cervical dorsal horns in the cat. J Comp Neurol 1986, 243:388-408.
84. Shigenaga Y., Doe K., Suemune S., Mitsuhiro Y., Tsuru K., Otani K., Shirana Y., Hosoi M., Yoshida A., Kagawa K. Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat - intra-axonal staining with HRP. Brain Res 1989, 505:91-110.
85. Shigenaga Y., Matano S., Kusuyama M., Sakai A. Cortical neurons responding to electrical stimulations of the rat's incisor pulp. Brain Res 1974, 67:153-156.
86. Shigenaga Y., Mitsuhiro Y., Shirana Y., Tsuru H. Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 1990, 514:219-237.
87. Shigenaga Y., Nakatani Z., Nishimori T., Suemune S., Kuroda R., Matano S. The cells of origin of cat trigeminothalamic projections: especially in the caudal medulla. Brain Res 1983, 277:201-222.
88. Shigenaga Y., Nishimura M., Suemune S., Nishimori T., Doe K., Tsuru H. Somatotopic organization of tooth pulp primary afferent neurons in the cat. Brain Res 1989, 477:66-89.
89. Shigenaga Y., Okamoto T., Nishimori T., Suemune S., Nasution I.D., Chen I.C., Tsuru K., Yoshida A., Tabuchi K., Hosoi M., Tsuru H. Oral and facial representation in the trigeminal principal and rostra1 spinal nuclei of the cat. J Comp Neurol 1986, 244:1-18.
90. Shigenaga Y., Sera M., Nishimori T., Suemune S., Nishimura M., Yoshida A., Tsuru K. The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 1988, 268:489-507.
91. Shigenaga Y., Suemune S., Nishimura M., Nishimori T., Sato H., Ishidori H., Yoshida A., Tsuru K., Tsuiki Y., Dateoka Y., Nasution I.D., Hosoi M. Topographic representation of lower and upper teeth within the trigeminal sensory nuclei of adult cat as demonstrated by the transganglionic transport of horseradish peroxidase. J Comp Neurol 1986, 251:299-316.
92. Spreafico R., Barbaresi P., Weinberg R.J., Rustioni A. SII-projecting neurons in the rat thalamus: a single- and double-retrograde-tracing study. Somatosens Res 1987, 4:359-375.
93. Steinmetz P.N., Roy A., Fitzgerald P.J., Hsiao S.S., Johnson K.O., Niebur E. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 2000, 444:187-190.
94. Swanson L.W. Brain maps: structure of the rat brain 1992, Elsevier, Amsterdam.
95. Takemura M., Sugimoto T., Sakai A. Topographic organization of central terminal region of different sensory branches of the rat mandibular nerve. Exp Neurol 1987, 96:540-557.
96. Takemura M., Sugimoto T., Shigenaga Y. Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Exp Neurol 1991, 111:324-331.
97. Tomita A., Kato T., Sato F., Haque T., Oka A., Yamamoto M., Ono T., Bae Y.-C., Maeda Y., Sessle B.J., Yoshida A. Somatotopic direct projections from orofacial areas of primary somatosensory cortex to pons and medulla, especially to trigeminal sensory nuclear complex, in rats. Neuroscience 2012, 200:166-185.
98. Torquati K., Pizzella V., Della Penna S., Franciotti R., Babiloni C., Romani G.L., Rossini P.M. " Gating" effects of simultaneous peripheral electrical stimulations on human secondary somatosensory cortex: a whole-head MEG study. NeuroImage 2003, 20:1704-1713.
99. Torvik A. The ascending fibers from the main trigeminal sensory nucleus. An experimental study in the cat. Am J Anat 1957, 100:1-15.
100. Valtschanoff J.G., Weinberg R.J., Rustioni A. Amino acid immunoreactivity in corticospinal terminals. Exp Brain Res 1993, 93:95-103.
101. van der Kooy D., Koda L.Y., McGinty J.F., Gerfen C.R., Bloom F.E. The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J Comp Neurol 1984, 224:1-24.
102. Voisin D.L., Doméjean-Orliaguet S., Chalus M., Dallel R., Woda A. Ascending connections from the caudal part to the oral part of the spinal trigeminal nucleus in the rat. Neuroscience 2002, 109:183-193.
103. Waite P.M.E. Trigeminal sensory system. The rat nervous system 2004, 817-851. Elsevier Academic Press, San Diego. 3rd ed. G. Paxinos (Ed.).
104. Wasaka T., Nakata H., Akatsuka K., Kida T., Inui K., Kakigi R. Differential modulation in human primary and secondary somatosensory cortices during the preparatory period of self initiated finger movement. Eur J Neurosci 2005, 22:1239-1247.
105. Weisberg J.A., Rustioni A. Differential projections of cortical sensorimotor areas upon the dorsal column nuclei of cats. J Comp Neurol 1979, 184:401-422.
106. Welker C., Sinha M.M. Somatotopic organization of SmII cerebral neocortex in albino rat. Brain Res 1972, 37:132-136.
107. Welker E., Hoogland P.V., Van der Loos H. Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse. Exp Brain Res 1988, 73:411-435.
108. Werner G., Whitsel B.L. Functional organization of the somatosensory cortex. Handbook of sensory physiology 1973, 621-700. Springer-Verlag, Berlin. A. Iggo (Ed.).
109. Westberg K.G., Clavelou P., Sandström G., Lund J.P. Evidence that trigeminal brainstem interneurons from subpopulations to produce different forms of mastication in the rabbit. J Neurosci 1998, 18:6466-6479.
110. Westberg K.G., Olsson K.å. Integration in trigeminal premotor interneurones in the cat. 1. Functional characteristics of neurons located in the subnucleus-γ of the oral nucleus of the spinal trigeminal tract. Exp Brain Res 1991, 84:102-114.
111. 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.
112. Wise S.P., Jones E.G. Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 1978, 178:187-208.
113. Wise S.P., Murray E.A., Coulter J.D. Somatotopic organization of corticospinal and corticotrigeminal neurons in the rat. Neuroscience 1979, 4:65-78.
114. Wold J.E., Brodal A. The projection of cortical sensorimotor regions onto the trigeminal nucleus in the cat. An experimental anatomical study. Neurobiology 1973, 3:353-375.
115. Woolston D.C., La Londe J.R., Gibson J.M. Corticofugal influences in the rat on responses of neurons in the trigeminal nucleus interpolaris to mechanical stimulation. Neurosci Lett 1983, 36:43-48.
116. Yasui Y., Breder C.D., Saper C.B., Cechetto D.F. Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 1991, 303:355-374.
117. Yoshida A., Taki I., Chang Z., Iida C., Haque T., Tomita A., Seki S., Yamamoto S., Masuda Y., Moritani M., Shigenaga Y. Corticofugal projections to the trigeminal motoneurons innervating antagonistic jaw muscles in rats as demonstrated by anterograde and retrograde tract-tracing. J Comp Neurol 2009, 514:368-386.
118. Zilles K. The cortex of the rat: a stereotaxic atlas 1985, Springer-Verlag, Berlin/Heidelberg/NY.