Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

Journal of Comparative Neurology

Volumn 509, Issue 3, 2008, Pages 239-258

  Kichula, Elizabeth A ^a   Huntley, George W ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Carbocyanine dyes; DH; PHA L; Somatosensory cortex; Synaptic plasticity; Ventrobasal nuclear complex

Indexed keywords

CARBOCYANINE; LEUKOAGGLUTININ;

ANATOMICAL VARIATION; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOARCHITECTURE; FEMALE; INFORMATION PROCESSING; INNERVATION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PHASEOLUS VULGARIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT; THALAMOCORTICAL TRACT; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; NERVE TRACT; THALAMUS POSTERIOR NUCLEUS; VIBRISSA;

ANIMALS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; POSTERIOR THALAMIC NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; SPECIES SPECIFICITY; VIBRISSAE;

EID: 47049110493     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21690     Document Type: Article

References (69)

1. Abdel-Majid RM, Leong WL, Schalkwyk LC, Smallman DS, Wong ST, Storm DR, Fine A, Dobson MJ, Guernsey DL, Neumann PE. 1998. Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex. Nat Genet 19:289-291.
2. Agmon A, Yang LT, O'Dowd DK, Jones EG. 1993. Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J Neurosci 13:5365-5382.
3. Agmon A, Yang LT, Jones EG, O'Dowd DK. 1995. Topological precision in the thalamic projection to neonatal mouse barrel cortex. J Neurosci 15:549-561.
4. Ahissar E, Sosnik R, Haidarliu S. 2000. Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406: 302-306.
5. Ahissar E, Sosnik R, Bagdasarian K, Haidarliu S. 2001. Temporal frequency of whisker movement. II. Laminar organization of cortical representations. J Neurophysiol 86:354-367.
6. Antonini A, Stryker MP. 1993. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J Neurosci 13:3549-3573.
7. Boylan CB, Bennett-Clarke CA, Crissman RS, Mooney RD, Rhoades RW. 2000. Clorgyline treatment elevates cortical serotonin and temporarily disrupts the vibrissae-related pattern in rat somatosensory cortex. J Comp Neurol 427:139-149.
8. Boylan CB, Kesterson KL, Bennett-Clarke CA, Chiaia NL, Rhoades RW. 2001. Neither peripheral nerve input nor cortical NMDA receptor activity are necessary for recovery of a disrupted barrel pattern in rat somatosensory cortex. Dev Brain Res 129:95-106.
9. Bureau I, Shepherd GM, Svoboda K. 2004. Precise development of functional and anatomical columns in the neocortex. Neuron 42:789-801.
10. Bureau I, von Saint Paul F, Svoboda K. 2006. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol 4:e382.
11. Catalano SM, Robertson RT, Killackey HP. 1991. Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proc Natl Acad Sci U S A 88:2999-3003.
12. Catalano SM, Robertson RT, Killackey HP. 1996. Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol 367:36-53.
13. Chiaia NL, Rhoades RW, Fish SE, Killackey HP. 1991. Thalamic processing of vibrissal information in the rat: II. Morphological and functional properties of medial ventral posterior nucleus and posterior nucleus neurons. J Comp Neurol 314:217-236.
14. Chmielowska J, Carvell GE, Simons DJ. 1989. Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285:325-338.
15. Crandall JE, Korde M, Caviness VS Jr. 1986. Somata of layer V projection neurons in the mouse barrelfield cortex are in preferential register with the sides and septa of the barrels. Neurosci Lett 67:19-24.
16. Deschenes M, Veinante P, Zhang ZW. 1998. The organization of corticothalamic projections: reciprocity versus parity. Brain Res Rev 28:286-308.
17. Diamond ME, Armstrong-James M, Ebner FF. 1992. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus. J Comp Neurol 318:462-476.
18. Donoghue JP, Parham C. 1983. The afferent connections of the lateral agranular field of the rat motor cortex. J Comp Neurol 217:76-88.
19. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, Frisen J, Kullander K, Flanagan JG, Polleux F, Vanderhaeghen P. 2003. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 39:453-465.
20. Erzurumlu RS, Jhaveri S. 1990. Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex. Dev Brain Res 56:229-234.
21. Fabri M, Burton H. 1991. Topography of connections between primary somatosensory cortex and posterior complex in rat: a multiple fluorescent tracer study. Brain Res 538:351-357.
22. Feldmeyer D, Roth A, Sakmann B. 2005. Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J Neurosci 25:3423-3431.
23. Frick A, Feldmeyer D, Helmstaedter M, Sakmann B. 2008. Monosynaptic connections between pairs of L5A pyramidal neurons in columns of juvenile rat somatosensory cortex. Cereb Cortex. 18:397-406.
24. Galazo MJ, Martinez-Cerdeno V, Porrero C, Clasca F. 2008. Embryonic and postnatal development of the layer I-directed ("matrix") thalamocortical system in the rat. Cereb Cortex. 18:344-363.
25. Godement P, Vanselow J, Thanos S, Bonhoeffer F. 1987. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101:697-713.
26. Goodman CS, Shatz CJ. 1993. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77-98.
27. Hoffer ZS, Arantes HB, Roth RL, Alloway KD. 2005. 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 488:82-100.
28. Inan M, Lu HC, Albright MJ, She WC, Crair MC. 2006. Barrel map development relies on protein kinase A regulatory subunit II beta-mediated cAMP signaling. J Neurosci 26:4338-4349.
29. Ince-Dunn G, Hall BJ, Hu SC, Ripley B, Huganir RL, Olson JM, Tapscott SJ, Ghosh A. 2006. Regulation of thalamocortical patterning and synaptic maturation by NeuroD2. Neuron 49:683-695.
30. Ivy GO, Killackey HP. 1981. The ontogeny of the distribution of callosal projection neurons in the rat parietal cortex. J Comp Neurol 195:367-389.
31. Jensen KF, Killackey HP. 1987. Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci 7:3529-3543.
32. Jin TE, Witzemann V, Brecht M. 2004. Fiber types of the intrinsic whisker muscle and whisking behavior. J Neurosci 24:3386-3393.
33. Kageyama GH, Robertson RT. 1993. Development of geniculocortical projections to visual cortex in rat: evidence early ingrowth and synaptogenesis. J Comp Neurol 335:123-148.
34. Kim U, Ebner FF. 1999. Barrels and septa: separate circuits in rat barrels field cortex. J Comp Neurol 408:489-505.
35. Koralek KA, Jensen KF, Killackey HP. 1988. Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex. Brain Res 463:346-351.
36. Lee LJ, Iwasato T, Itohara S, Erzurumlu RS. 2005. Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol 485:280-292.
37. Lieske V, Bennett-Clarke CA, Rhoades RW. 1999. Effects of serotonin on neurite outgrowth from thalamic neurons in vitro. Neuroscience 90: 967-974.
38. Lin CS, Nicolelis MA, Schneider JS, Chapin JK. 1990. A major direct GABAergic pathway from zona incerta to neocortex. Science 248:1553-1556.
39. Lotto B, Upton L, Price DJ, Gaspar P. 1999. Serotonin receptor activation enhances neurite outgrowth of thalamic neurones in rodents. Neurosci Lett 269:87-90.
40. Lu SM, Lin RC. 1993. Thalamic afferents of the rat barrel cortex: a light- and electron- microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens Mot Res 10:1-16.
41. Lund RD, Mustari MJ. 1977. Development of the geniculocortical pathway in rats. J Comp Neurol 173:289-306.
42. Maier DL, Mani S, Donovan SL, Soppet D, Tessaroll L, McCasland JS, Meiri KF. 1999. Disrupted cortical map and absence of corticals barrels in growth-associated protein (GAP)-43 knockout mice. Proc Natl Acad Sci U S A 96:9397-9402.
43. Miller B, Blake NM, Erinjeri JP, Reistad CE, Sexton T, Admire P, Woolsey TA. 2001. Postnatal growth of intrinsic connections in mouse barrel cortex. J Comp Neurol 436:17-31.
44. Mitchell BD, Macklis JD. 2005. Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice. J Comp Neurol 482:17-32.
45. Nothias F, Peschanski M, Besson JM. 1988. Somatotopic reciprocal connections between the somatosensory cortex and the thalamic Po nucleus in the rat. Brain Res 447:169-174.
46. O'Leary DD, Stanfield BB, Cowan WM. 1981. Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. Brain Res 227:607-617.
47. Porter LL, White EL. 1983. Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse. J Comp Neurol 214:279-289.
48. Rebsam A, Seif I, Gaspar P. 2002. Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase in knock-out mice. J Neurosci 22:8541-8552.
49. Rhoades RW, Bennett-Clarke CA, Shi MY, Mooney RD. 1994. Effects of 5-HT on thalamocortical synaptic transmission in the developing rat. J Neurophysiol 72:2438-2450.
50. Rhoades RW, Crissman RS, Bennett-Clarke CA, Killackey HP, Chiaia NL. 1996. Development and plasticity of local intracortical projections within the vibrissae representation of the rat primary somatosensory cortex. J Comp Neurol 370:524-535.
51. Rice FL. 1985. Gradual changes in the structure of the barrels during maturation of the primary somatosensory cortex in the rat. J Comp Neurol 236:496-503.
52. Rice FL, Van der Loos H. 1977. Development of the barrels and barrel field in the somatosensory cortex of the mouse. J Comp Neurol 171:545-560.
53. Rice FL, Gomez C, Barstow C, Burnet A, Sands P. 1985. A comparative analysis of the development of the primary somatosensory cortex: interspecies similarities during barrel and laminar development. J Comp Neurol 236:477-495.
54. Saper CB. 1985. Organization of cerebral cortical afferent systems in the rat. II. Hypothalamocortical projections. J Comp Neurol 237:21-46.
55. Schlaggar BL, O'Leary DD. 1994. Early development of the somatotopic map and barrel patterning in rat somatosensory cortex. J Comp Neurol 346:80-96.
56. Senft SL, Woolsey TA. 1991. Growth of thalamic afferents into mouse barrel cortex. Cereb Cortex 1:308-335.
57. Shepherd GM, Svoboda K. 2005. Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25:5670-5679.
58. Shimogori T, Grove EA. 2005. Fibroblast growth factor 8 regulates neocortical guidance of area-specific thalamic innervation. J Neurosci 25: 6550-6560.
59. Spreafico R, Barbaresi P, Weinberg RJ, Rustioni A. 1987. SII-projecting neurons in the rat thalamus: a single- and double-retrograde-tracing study. Somatosens Res 4:359-375.
60. Van der Loos H, Woolsey TA. 1973. Somatosensory cortex: structural alterations following early injury to sense organs. Science 179:395-398.
61. Vercelli A, Repici M, Garbossa D, Grimaldi A. 2000. Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51:11-28.
62. Vitalis T, Cases O, Callebert J, Launay JM, Price DJ, Seif I, Gaspar P. 1998. Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex: determination of a sensitive developmental period. J Comp Neurol 393:169-184.
63. Welker C, Woolsey TA. 1974. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol 158:437-453.
64. Wise SP, Jones EG. 1977. Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol 175:129-157.
65. Wise SP, Jones EG. 1978. Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178:187-208.
66. Wong-Riley MTT. 1979. Changes in the visual system of monocularly sutured or enucleated kittens demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11-28.
67. 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.
68. Yu C, Derdikman D, Haidarliu S, Ahissar E. 2006. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol 4:e124.
69. Zhang ZW, Deschenes M. 1998. Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb Cortex 8:428-436.