Quantitative analysis of synaptic distribution along thalamocortical axons in adult mouse barrels

Journal of Comparative Neurology

Volumn 479, Issue 1, 2004, Pages 56-69

  White, Edward L ^a   Weinfeld, Elizabeth ^a   Lev, Dmitri L ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

3D reconstruction; Serial thin sections; Synaptic organization

Indexed keywords

DEXTRAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC SPINE; ELECTRON MICROSCOPY; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SOMATOSENSORY CORTEX; SYNAPSE; SYNAPTIC MEMBRANE; THALAMOCORTICAL TRACT; THALAMUS; TISSUE SECTION;

ANIMALS; IMAGING, THREE-DIMENSIONAL; MICE; NEURAL PATHWAYS; NEURONS, AFFERENT; SOMATOSENSORY CORTEX; SYNAPSES; THALAMUS;

EID: 4644334926     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20300     Document Type: Article

References (88)

1. Adams JC. 1981. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775.
2. Anderson JC, Dehay C, Friedlander MJ, Martin KAC, Nelson JC. 1992. Synaptic connections of physiologically identified geniculocortical axons in kitten cortical area 17. Proc R Soc Lond B Biol Sci 250:187-194.
3. Arnold PB, Li CX, Waters RS. 2001. Thalamocortical arbors extend beyond single cortical barrels: an in vivo intracellular tracing study in rat. Exp Brain Res 136:152-168.
4. Bernardo KL, Woolsey TA. 1987. Axonal trajectories between mouse somatosensory thalamus and cortex. J Comp Neurol 258:542-564.
5. Castro-Alamancos MA, Connors BW. 1997. Thalamocortical synapses. Prog Neurobiol 51:581-606.
6. Chicurel ME, Harris KM. 1992. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 325:169-182.
7. Cipolloni PB, Peters A. 1983. The termination of callosal fibres in the auditory cortex of the rat. A combined Golgi-electron microscope and degeneration study. J Neurocytol 12:713-726.
8. Cipolloni PB, Hersch SM, White EL. 1985. The use of lectin transport as an anterograde marker for electron microscopy. Neurosci Lett 58:43-47.
9. Colonnier M. 1968. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268-287.
10. Colonnier M. 1981. The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In: Schmitt FO, Worden FG, editors. The organization of the cerebral cortex. Cambridge: MIT Press. p 125-153.
11. Cunningham ET Jr, LeVay S. 1986. Laminar and synaptic organization of the projection from the thalamic nucleus centralis to primary visual cortex in the cat. J Comp Neurol 254:65-77.
12. Czeiger D, White EL. 1993. Synapses of extrinsic and intrinsic origin made by callosal projection neurons in mouse visual cortex. J Comp Neurol 330:502-513.
13. Davis TL, Sterling P. 1979. Microcircuitry of cat visual cortex: classification of neurons in layer IV of area 17, and identification of the patterns of lateral geniculate input. J Comp Neurol 188:599-628.
14. DeFelipe J, Fairén A. 1993. A simple and reliable method for correlative light and electron microscopic studies. J Histochem Cytochem 41:769-772.
15. DeFelipe J, Elston GN, Fujita I, Fuster J, Harrison KH, Hof PR, Kawabuchi H, Martin KAC, Rockland KS, Thomson AM, Wang SS-H, White EL, Yuste R. 2002. Neocortical circuits: evolutionary aspects and specificity versus non-specificity of synaptic connections. Remarks, main conclusions and general comments and discussion. J Neurocytol 31: 387-416.
16. Del Rio M, DeFelipe J. 1997. Synaptic connections of calretinin- immunoreactive neurons in the human neocortex. J Neurosci 17:5143-5154.
17. Dykes RW, Ruest A. 1986. What makes a map in somatosensory cortex? In: Jones EG, Peters A, editors. Cerebral cortex, vol 5: Sensory-motor areas of cortical connectivity. New York: Plenum Press. p 1-29.
18. Einstein G, Davis TL, Sterling P. 1987. Ultrastructure of synapses from the A-laminae of the lateral geniculate nucleus in layer IV of the cat striate cortex. J Comp Neurol 260:63-75.
19. Elhanany E, White EL. 1990. Intrinsic circuitry: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J Comp Neurol 291:43-54.
20. Fairén A, Peters A, Saldanha J. 1977. A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J Neurocytol 6:311-337.
21. Fox K, Schlaggar BL, Glazewski S, O'Leary DD. 1996. Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex. Proc Natl Acad Sci U S A 93:5584-5589.
22. Franklin KBJ, Paxinos G. 1997. The mouse brain in stereotaxic coordinates. New York.: Academic Press.
23. Freund TF, Martin KAC, Soltész I, Somogyi P, Whitteridge D. 1989. Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. J Comp Neurol 289:315-336.
24. Friedman HV, Bresler T, Garner CC, Ziv NE. 2000. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
25. Garey LJ, Powell TPS. 1971. An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc R Soc Lond B Biol Sci 179:41-63.
26. Heimer L, Zaborszky L (eds). 1989. Neuroanatomical tract-tracing methods 2. New York: Plenum Press. 408 p.
27. Herrmann K, Antonini A, Shatz CJ. 1994. Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur J Neurosci 6:1729-1742.
28. Hersch SM, White EL. 1981. Thalamocortical synapses with corticothalamic projection neurons in mouse SmI cortex: electron microscopic demonstration of a monosynaptic feedback loop. Neurosci Lett 24:297-210.
29. Hubel DH, Wiesel TN. 1977. Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci 198:1-59.
30. 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.
31. Jones EG, Powell TPS. 1970. An electron microscopic study of the laminar pattern and mode of termination of afferent fibre pathways in the somatic sensory cortex of the cat. Philos Trans R Soc Lond B Biol Sci 257:45-62.
32. Keller A. 1995. Synaptic organization of the barrel cortex. In: Jones EG, Diamond IT, editors. Cerebral cortex. New York: Plenum Press. p 221-262.
33. Keller A, White EL, Cipolloni PB. 1985. The identification of thalamocortical axon terminals in barrels of mouse SmI cortex using immunohistochemistry of anterogradely transported lectin (Phaseolus vulgaris lecoagglutinin). Brain Res 343:159-165.
34. Killackey HP. 1973. Anatomical evidence for cortical subdivisions based on vertically discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat. Brain Res 51:326-331.
35. Killackey HP, Leshin S. 1975. The organization of specific thalamocortical projections to the posteromedial barrel subfield of the rat somatic sensory cortex. Brain Res 86:469-472.
36. Lev DL, Weinfeld EB, White EL. 2002. Synaptic patterns of thalamocortical afferents in mouse barrels at postnatal day 11. J Comp Neurol 442:63-77.
37. LeVay S. 1986. Synaptic organization of claustral and geniculate afferents to the visual cortex of the cat. J Neurosci 6:3564-3575.
38. LeVay S, Gilbert CD. 1976. Laminar patterns of the geniculocortical projections in the cat. Brain Res 113:1-19.
39. Lorente de No R. 1938. The physiology of the nervous system. In: Fulton JF, editor. The physiology of the nervous system. New York: Oxford University Press. p 291-329.
40. Lu S-M, Lin RC-S. 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. McGuire BA, Hornung J-P, Gilbert CD, Wiesel TN. 1984. Patterns of synaptic input to layer 4 of cat striate cortex. J Neurosci 4:3021-3033.
42. Mountcastle VB. 1977. The columnar organization of the neocortex. Brain 120:701-722.
43. Mountcastle VB. 1978. An organizing principle for cerebral function: The unit module and the distributed system. In: Edelman GM, Mountcastle VB, editors. The mindful brain. Cambridge: MIT Press. p 7-50.
44. Mountcastle VB. 1979. An organizing principle for cerebral function: the unit module and the distributed system. The neurosciences fourth study program. Cambridge: MIT Press. p 21-42.
45. Mountcastle V. 1995. The evolution of ideas concerning the function of the neocortex. Cereb Cortex 5:289-295.
46. Papadopoulos GC, Dori I. 1993. DiI labeling combined with conventional immunocytochemical techniques for correlated light and electron microscopic studies. J Neurosci Methods 46:251-258.
47. Peters A, Feldman ML. 1976. The projection of the lateral geniculate nucleus to area 17 of rat cerebral cortex. I. General description. J Neurocytol 5:63-84.
48. Peters A, Palay SL. 1996. The morphology of synapses. J Neurocytol 25:687-700.
49. Peters A, Proskauer CC. 1980. Synaptic relations between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study. J Neurocytol 9:163-183.
50. Peters A, White EL, Fairén A. 1977. Synapses between identified neuronal elements. An electron microscopic demonstration of degenerating axon terminals synapsing with Golgi impregnated neurons. Neurosci Lett 6:171-175.
51. Pinto DJ, Brumberg JC, Simons DJ. 2000. Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83:1158-1166.
52. Ralston HJ III. 1990. Analysis of neuronal networks: a review of techniques for labeling axonal projections. J Electron Microsc Tech 15:322-331.
53. Rice FL. 1995. Comparative aspects of barrel structure and development. In: Jones EG, Diamond IT, editors. Cerebral cortex. New York: Plenum Press. p 1-75.
54. Saporta S, Kruger L. 1977. The organization of thalamocortical relay neurons in the rat ventrobasal complex studied by retrograde transport of horseradish peroxidase. J Comp Neurol 174:187-208.
55. Schlaggar BL, O'Leary DDM. 1994. Early development of the somatotopic map and barrel patterning in rat somatosensory cortex. J Comp Neurol 346:80-96.
56. Shanks MF, Powell TPS. 1981. An electron microscopic study of the termination of thalamocortical fibers in areas 3b, 1 and 2 of the somatic sensory cortex of the monkey. Brain Res 218:35-47.
57. Sidman RL, Angevin JB Jr, Pierce ET. 1971. Atlas of the mouse brain and spinal cord. Cambridge: University Press.
58. Sloper JJ. 1973. An electron microscope study of the termination of afferent connections to the primate motor cortex. J Neurocytol 2:361-368.
59. Sloper JJ, Powell TPS. 1979. An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos Trans R Soc Lond B Biol Sci 285:199-225.
60. Smith LM, Ebner FF, Colonnier M. 1980. The thalamocortical projection in Pseudemys turtles: a quantitative electron microscopic study. J Comp Neurol 190:445-461.
61. Staiger JF, Kötter R, Zilles K, Luhmann HJ. 1999. Connectivity in the somatosensory cortex of the adolescent rat: an in vitro biocytin study. Anat Embryol (Berl) 199:357-365.
62. Strick PL, Sterling P. 1974. Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscope study. J Comp Neurol 153:77-106.
63. Tigges M, Tigges J. 1979. Types of degenerating geniculocortical axon terminals and their contribution to layer IV of area 17 in the squirrel monkey (Samiri). Cell Tissue Res 196:471-486.
64. Van der Loos H. 1976. Barreloids in mouse somatosensory thalamus. Neurosci Lett 2:1-6.
65. Veenman CL, Reiner A, Honig MG. 1992. Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Methods 41:239-254.
66. White EL. 1973. Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation. Brain Res 40:299-313.
67. White EL. 1978. Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals: A combined Golgi-electron microscopic and degeneration study. J Comp Neurol 181:627-662.
68. White EL. 1979. Thalamocortical synaptic relations: a review with emphasis on the projection of specific thalamic nuclei to the primary sensory areas of the neocortex. Brain Res Rev 1:275-311.
69. White EL. 1981. Thalamocortical synaptic relations. In: Schmitt FO, Worden FG, editors. The organization of the cerebral cortex. Cambridge: MIT Press. p 153-161.
70. White EL. 1986. Termination of thalamic afferents in the cerebral cortex. In: Jones EG, Peters A, editors. Cerebral cortex. New York: Plenum Press. p 271-289.
71. White EL. 1987. Thalamocortical interactions. In: Encyclopedia of neuroscience. Boston: Birkhauser Publ. p 1202-1204.
72. White EL. 1989a. Cortical circuits synaptic organization of the cerebral cortex: structure, function, and theory. Boston: Birkhauser Publ. p 1-223.
73. White EL. 1989b. Cell types. In: Cortical circuits synaptic organization of the cerebral cortex; structure, function and theory, 1st ed. Boston: Birkhauser Publ. p 19-45.
74. White EL. 1989c. Synaptic connections between identified elements. In: Cortical circuits synaptic organization of the cerebral cortex; structure, function and theory, 1st ed. Boston: Birkhauser. p 46-82.
75. White EL. 2002. Specificity of cortical synaptic connectivity; emphasis on perspectives gained from quantitative electron microscopy. J Neurocytol 31:183-193.
76. White EL, Czeiger D. 1991. Synapses made by axons of callosal projection neurons in mouse somatosensory cortex: emphasis on intrinsic connections. J Comp Neurol 303:233-244.
77. White EL, DeAmicis R. 1977. Afferent and efferent projections of the region in mouse SmI cortex which contains the posteromedial barrel subfield. J Comp Neurol 175:455-481.
78. White EL, Hersch SM. 1981. Thalamocortical synapses of pyramidal cells which project from SmI to MsI cortex in the mouse. J Comp Neurol 198:167-181.
79. White EL, Keller A. 1987. Intrinsic circuitry involving the local axonal collaterals of corticothalamic projection cells in mouse SmI cortex. J Comp Neurol 262:13-26.
80. White EL, Keller A. 1989. An integrative view of cortical circuitry. Cortical circuits synaptic organization of the cerebral cortex; structure, function, and theory, 1st ed. Boston: Birkhauser Publ. p 179-206.
81. White EL, Rock MP. 1980. Three dimensional aspects and synaptic relationships of a Golgi impregnated spiny stellate cell reconstructed from serial thin sections. J Neurocytol 9:615-636.
82. White EL, Rock MP. 1981. A comparison of thalamocortical and other synaptic inputs to dendrites of two non-spiny neurons in a single barrel of mouse SmI cortex. J Comp Neurol 195:265-277.
83. White EL, Hersch SM, Rock MP. 1980. Synaptic sequences in mouse SmI cortex involving pyramidal cells labeled by retrograde filling with horseradish peroxidase. Neurosci Lett 19:149-154.
84. Williams MA, Meek GA. 1966. Studies on thickness variation in ultrathin sections. J R Microsc Soc 85:337.
85. Winfield DA, Powell TPS. 1983. Laminar cell counts and geniculo-cortical boutons in area 17 of cat and monkey. Brain Res 277:223-229.
86. Winfield DA, Brooke RNL, Sloper JJ, Powell TPS. 1981. A combined Golgi-electron microscopic study of the synapses made by the proximal axon and recurrent collaterals of a pyramidal cell in the somatic sensory cortex of the monkey. Neuroscience 6:1217-1230.
87. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res 17:205-242.
88. Zantua JB, Wasserstrom SP, Arends JJA, Jacquin MF, Woolsey TA. 1996. Postnatal development of mouse "whisker" thalamus: ventroposterior medial nucleus (VPM), barreloids, and their thalamocortical relay neurons. Somatosens Mot Res 13:307-322.