Organization of the spinal trigeminal nucleus in star-nosed moles

Journal of Comparative Neurology

Volumn 522, Issue 14, 2014, Pages 3335-3350

  Sawyer, Eva K ^a   Leitch, Duncan B ^b,c   Catania, Kenneth C ^c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Barrelettes; Caudalis; Evolution; Interpolaris; RRID: nif 0000 23420; Somatosensory

Indexed keywords

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MAPPING; BRAIN STEM; CONDYLURA CRISTATA; CONTROLLED STUDY; FACE; HISTOLOGY; JUVENILE; MOLE (INSECTIVORA); NONHUMAN; PRINCIPAL SENSORY NUCLEUS; PRIORITY JOURNAL; RECEPTIVE FIELD; SUBNUCLEUS CAUDALIS; SUBNUCLEUS INTERPOLARIS; THREE DIMENSIONAL IMAGING; TRIGEMINAL NUCLEUS; ANATOMY AND HISTOLOGY; ANIMAL; ELECTROSTIMULATION; FEMALE; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; MALE; METABOLISM; NERVE TRACT; NEWBORN; PHYSIOLOGY; PREGNANCY; SENSATION;

CYTOCHROME C OXIDASE;

ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; ELECTRIC STIMULATION; ELECTRON TRANSPORT COMPLEX IV; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MOLES; NEURAL PATHWAYS; PREGNANCY; SENSATION; TRIGEMINAL NUCLEUS, SPINAL;

EID: 84904549625     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23605     Document Type: Article

References (59)

1. Amano N, Hu JW, Sessle BJ. 1986. Responses of neurons in feline trigeminal subnucleus caudalis (medullary dorsal horn) to cutaneous, intraoral, and muscle afferent stimuli. J Neurophysiol 55:227-243.
2. Anstrom KE. 1953. On the central course of afferent fibres in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse. Acta Physiol Scand 106(Suppl):209-320.
3. Arvidsson J. 1982. Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 211:84-92.
4. Ashwell KW, Hardman CD, Paxinos G. 2006. Cyto- and chemoarchitecture of the sensory trigeminal nuclei of the echidna, platypus and rat. J Chemical Neuroanat 31:81-107.
5. Belford GR, Killackey HP. 1979. Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 183:305-321.
6. Bosman LW, Houweling AR, Owens CB, Tanke N, Shevchouk OT, Rahmati N, Teunissen WH, Ju C, Gong W, Koekkoek SK, De Zeeuw CI. 2011. Anatomical pathways involved in generating and sensing rhythmic whisker movements. Front Integr Neurosci 5:53.
7. Carroll EW, Wong-Riley MT. 1984. Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. J Comp Neurol 222:1-17.
8. Catania KC. 1996. Ultrastructure of the Eimer's organ of the star-nosed mole. J Comp Neurol 365:343-354.
9. Catania KC. 2001. Early development of a somatosensory fovea: a head start in the cortical space race? Nat Neurosci 4:353-354.
10. Catania KC, Kaas JH. 1995. Organization of the somatosensory cortex of the star-nosed mole. J Comp Neurol 351:549-567.
11. Catania KC, Kaas JH. 1997. Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation. J Comp Neurol 387:215-233.
12. Catania KC, Remple FE . 2004. Tactile foveation in the star-nosed mole. Brain Behav Evol 63:1-12.
13. Catania KC, Leitch DB, Gauthier D. 2011. A star in the brainstem reveals the first step of cortical magnification. Plos One 6(7).
14. Catania KC, Catania EH, Sawyer EK, Leitch DB. 2013. Barrelettes without barrels in the american water shrew. Plos One 8:e65975.
15. Craner SL, Ray RH . 1991. Somatosensory cortex of the neonatal pig: I. Topographic organization of the primary somatosensory cortex (SI). J Comp Neurol 306:24-38.
16. DaSilva AF, Becerra L, Makris N, Strassman AM, Gonzalez RG, Geatrakis N, Borsook D. 2002. Somatotopic activation in the human trigeminal pain pathway. J Neurosci 22:8183-8192.
17. Davies AJ, North RA. 2009. Electrophysiological and morphological properties of neurons in the substantia gelatinosa of the mouse trigeminal subnucleus caudalis. Pain 146:214-221.
18. Dejerine J. 1985. Classics in neurology-intermittent claudication of the spinal-cord (reprinted from Semiologie des Affections du Systeme Nerveux P9:267-269, 1914). Neurology 35:860-860.
19. Devoize L, Domejean S, Melin C, Raboisson P, Artola A, Dallel R. 2010. Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat: a neuroanatomical substrate for reciprocal orofacial-cervical interactions. Brain Res 1343:75-82.
20. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E. 2008. "Where" and "what" in the whisker sensorimotor system. Nat Rev Neurosci 9:601-612.
21. DiCarlo JJ, Johnson KO, Hsiao SS. 1998. Structure of receptive fields in area 3b of primary somatosensory cortex in the alert monkey. J Neurosci 18:2626-2645.
22. Erzurumlu RS, Murakami Y, Rijli FM. 2010. Mapping the face in the somatosensory brainstem. Nat Rev Neurosci 11:252-263.
23. Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61.
24. Friedberg MH, Lee SM, Ebner FF. 1999. Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 81:2243-2252.
25. Furuta T, Timofeeva E, Nakamura K, Okamoto-Furuta K, Togo M, Kaneko T, Deschenes M. 2008. Inhibitory gating of vibrissal inputs in the brainstem. J Neurosci 28:1789-1797.
26. Gallyas F. 1979. Silver staining of myelin by means of physical development. Neurol Res 1:203-209.
27. Gerard MW. 1923. Afferent impulses of the trigeminal nerve. AMA Arch Neurol Psychiatry 9:306-338.
28. Gerhold KA, Pellegrino M, Tsunozaki M, Morita T, Leitch DB, Tsuruda PR, Brem RB, Catania KC, Bautista DM. 2013. The star-nosed mole reveals clues to the molecular basis of mammalian touch. Plos One 8:e55001.
29. Hamilton WB. 1931. Habits of the star-nosed mole, Condylura cristata. J Mammal 12:345-355.
30. Hattox AM, Priest CA, Keller A. 2002. Functional circuitry involved in the regulation of whisker movements. J Comp Neurol 442:266-276.
31. Hayashi H, Sumino R, Sessle BJ. 1984. Functional organization of trigeminal subnucleus interpolaris: nociceptive and innocuous afferent inputs, projections to thalamus, cerebellum, and spinal cord, and descending modulation from periaqueductal gray. J Neurophysiol 51:890-905.
32. Henderson TAJ. 1995. What makes subcortical barrels? Jegdi T, editor. Cerebral cortex, the barrel cortex in rodents, vol 11. New York: Plenum. p 123-178.
33. Hu JW, Dostrovsky JO, Sessle BJ. 1981. 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 45:173-192.
34. Jacquin MF, Semba K, Egger MD, Rhoades RW. 1983. Organization of HRP-labeled trigeminal mandibular primary afferent neurons in the rat. J Comp Neurol 215:397-420.
35. Jacquin MF, Renehan WE, Mooney RD, Rhoades RW. 1986a. Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 55:1153-1186.
36. Jacquin MF, Woerner D, Szczepanik AM, Riecker V, Mooney RD, Rhoades RW. 1986b. Structure-function relationships in rat brainstem subnucleus interpolaris. I. Vibrissa primary afferents. J Comp Neurol 243:266-279.
37. Lee S, Carvell GE, Simons DJ. 2008. Motor modulation of afferent somatosensory circuits. Nat Neurosci 11:1430-1438.
38. Ma PM. 1991. The barrelettes-architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. I. Normal structural organization. J Comp Neurol 309:161-199.
39. Marasco PD, Tsuruda PR, Bautista DM, Julius D, Catania KC. 2006. Neuroanatomical evidence for segregation of nerve fibers conveying light touch and pain sensation in Eimer's organ of the mole. Proc Natl Acad Sci U S A 103:9339-9344.
40. Nash PG, Macefield VG, Klineberg IJ, Murray GM, Henderson LA. 2009. Differential activation of the human trigeminal nuclear complex by noxious and non-noxious orofacial stimulation. Hum Brain Mapping 30:3772-3782.
41. Nguyen QT, Kleinfeld D. 2005. Positive feedback in a brainstem tactile sensorimotor loop. Neuron 45:447-457.
42. Olszewski J. 1950. On the anatomical and functional organization of the spinal trigeminal nucleus. J Comp Neurol 92:401-413.
43. Panneton WM, Burton H. 1981. Corneal and periocular representation within the trigeminal sensory complex in the cat studied with transganglionic transport of horseradish peroxidase. J Comp Neurol 199:327-344.
44. Phelan KD, Falls WM . 1989. An analysis of the cyto- and myeloarchitectonic organization of trigeminal nucleus interpolaris in the rat. Somatosens Mot Res 6:333-366.
45. Pons TP, Wall JT, Garraghty PE, Cusick CG, Kaas JH. 1987. Consistent features of the representation of the hand in area 3b of macaque monkeys. Somatosens Res 4:309-331.
46. Price DD, Dubner R, Hu JW. 1976. Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J Neurophysiol 39:936-953.
47. Ramon y Cajal S. 1896. Beitrag zum Studium der Medulla oblongata, des Kleinhirns uud des Ursprungs der Gehirnnerven. Leipzig: J.A. Barth. 1-139 p.
48. Rustioni A, Sanyal S, Kuypers HG. 1971. A histochemical study of the distribution of the trigeminal divisions in the substantia gelatinosa of the rat. Brain Res 32:45-52.
49. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
50. Shigenaga Y, Chen IC, Suemune S, Nishimori T, Nasution ID, Yoshida A, Sato H, Okamoto T, Sera M, Hosoi M. 1986. Oral and facial representation within the medullary and upper cervical dorsal horns in the cat. J Comp Neurol 243:388-408.
51. Silver R, Witkovsky P. 1973. Functional characteristics of single units in the spinal trigeminal nucleus of the pigeon. Brain Behav Evol 8:287-303.
52. Sur M, Merzenich MM, Kaas JH. 1980. Magnification, receptive-field area, and "hypercolumn" size in areas 3b and 1 of somatosensory cortex in owl monkeys. J Neurophysiol 44:295-311.
53. Timofeeva E, Lavallée P, Arsenault D, Deschênes M . 2004. Synthesis of multiwhisker-receptive fields in subcortical stations of the vibrissa system. J Neurophysiol 91:1510-1515.
54. Torvik A. 1956. Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures; an experimental study in the rat. J Comp Neurol 106:51-141.
55. Van Der Loos H. 1976. Barreloids in mouse somatosensory thalamus. Neurosci Lett 2:1-6.
56. Vega-Bermudez F, Johnson KO. 1999. SA1 and RA receptive fields, response variability, and population responses mapped with a probe array. J Neurophysiol 81:2701-2710.
57. Woolsey TA, Van der Loos H. 1970. 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 Res 17:205-242.
58. Xerri C, Merzenich MM, Peterson BE, Jenkins W. 1998. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol 79:2119-2148.
59. Yokota T, Nishikawa N. 1980. Reappraisal of somatotopic tactile representation within trigeminal subnucleus caudalis. J Neurophysiol 43:700-712.