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. 1992 Mar 1;89(5):1832–1836. doi: 10.1073/pnas.89.5.1832

Cortical local circuit axons do not mature after early deafferentation.

J S McCasland 1, K L Bernardo 1, K L Probst 1, T A Woolsey 1
PMCID: PMC48547  PMID: 1542679

Abstract

The processes underlying development, refinement, and retention of the intracortical connections critical for the function of the mammalian brain are unknown. Horseradish peroxidase-labeled fibers in mouse somatosensory barrel cortex, which is patterned like the whiskers on the contralateral face from which it receives inputs, were evaluated by automated image analysis. The sensory nerve to the whiskers was sectioned on postnatal day 7, after the whisker map is set. The deprived barrel cortices, examined in adults, showed drastically diminished intracortical projections relative to normal controls, although the map of the whiskers in the cortex was unchanged. This demonstrates anatomically that the normal pattern of intracortical connections, like the normal sensory map, is dependent upon the sensory periphery four synapses away.

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Selected References

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  1. Belford G. R., Killackey H. P. The sensitive period in the development of the trigeminal system of the neonatal rat. J Comp Neurol. 1980 Sep 15;193(2):335–350. doi: 10.1002/cne.901930203. [DOI] [PubMed] [Google Scholar]
  2. Bernardo K. L., Ma P. M., Woolsey T. A. In vitro labeling of axonal projections in the mammalian central nervous system. J Neurosci Methods. 1986 Apr;16(2):89–101. doi: 10.1016/0165-0270(86)90042-7. [DOI] [PubMed] [Google Scholar]
  3. Bernardo K. L., McCasland J. S., Woolsey T. A. Local axonal trajectories in mouse barrel cortex. Exp Brain Res. 1990;82(2):247–253. doi: 10.1007/BF00231244. [DOI] [PubMed] [Google Scholar]
  4. Bernardo K. L., McCasland J. S., Woolsey T. A., Strominger R. N. Local intra- and interlaminar connections in mouse barrel cortex. J Comp Neurol. 1990 Jan 8;291(2):231–255. doi: 10.1002/cne.902910207. [DOI] [PubMed] [Google Scholar]
  5. Blakemore C. The conditions required for the maintenance of binocularity in the kitten's visual cortex. J Physiol. 1976 Oct;261(2):423–444. doi: 10.1113/jphysiol.1976.sp011566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Callaway E. M., Katz L. C. Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):745–749. doi: 10.1073/pnas.88.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Callaway E. M., Katz L. C. Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurosci. 1990 Apr;10(4):1134–1153. doi: 10.1523/JNEUROSCI.10-04-01134.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Daw N. W., Fox K., Sato H., Czepita D. Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol. 1992 Jan;67(1):197–202. doi: 10.1152/jn.1992.67.1.197. [DOI] [PubMed] [Google Scholar]
  9. Durham D., Woolsey T. A. Effects of neonatal whisker lesions on mouse central trigeminal pathways. J Comp Neurol. 1984 Mar 1;223(3):424–447. doi: 10.1002/cne.902230308. [DOI] [PubMed] [Google Scholar]
  10. Elhanany E., White E. L. Intrinsic circuitry: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J Comp Neurol. 1990 Jan 1;291(1):43–54. doi: 10.1002/cne.902910105. [DOI] [PubMed] [Google Scholar]
  11. Hendry S. H., Jones E. G., Emson P. C., Lawson D. E., Heizmann C. W., Streit P. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res. 1989;76(2):467–472. doi: 10.1007/BF00247904. [DOI] [PubMed] [Google Scholar]
  12. Hibbard L. S., Hawkins R. A. Objective image alignment for three-dimensional reconstruction of digital autoradiograms. J Neurosci Methods. 1988 Nov;26(1):55–74. doi: 10.1016/0165-0270(88)90129-x. [DOI] [PubMed] [Google Scholar]
  13. Hirsch J. A., Gilbert C. D. Synaptic physiology of horizontal connections in the cat's visual cortex. J Neurosci. 1991 Jun;11(6):1800–1809. doi: 10.1523/JNEUROSCI.11-06-01800.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Keller A., White E. L. Triads: a synaptic network component in the cerebral cortex. Brain Res. 1989 Sep 4;496(1-2):105–112. doi: 10.1016/0006-8993(89)91056-1. [DOI] [PubMed] [Google Scholar]
  15. LeVay S., Wiesel T. N., Hubel D. H. The development of ocular dominance columns in normal and visually deprived monkeys. J Comp Neurol. 1980 May 1;191(1):1–51. doi: 10.1002/cne.901910102. [DOI] [PubMed] [Google Scholar]
  16. Lund J. S. Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci. 1988;11:253–288. doi: 10.1146/annurev.ne.11.030188.001345. [DOI] [PubMed] [Google Scholar]
  17. Luskin M. B., Shatz C. J. Neurogenesis of the cat's primary visual cortex. J Comp Neurol. 1985 Dec 22;242(4):611–631. doi: 10.1002/cne.902420409. [DOI] [PubMed] [Google Scholar]
  18. Löwel S., Singer W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science. 1992 Jan 10;255(5041):209–212. doi: 10.1126/science.1372754. [DOI] [PubMed] [Google Scholar]
  19. Ma P. M., Woolsey T. A. Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. Brain Res. 1984 Jul 23;306(1-2):374–379. doi: 10.1016/0006-8993(84)90390-1. [DOI] [PubMed] [Google Scholar]
  20. Martin K. A., Friedlander M. J., Alones V. Physiological, morphological, and cytochemical characteristics of a layer 1 neuron in cat striate cortex. J Comp Neurol. 1989 Apr 15;282(3):404–414. doi: 10.1002/cne.902820307. [DOI] [PubMed] [Google Scholar]
  21. Matsubara J. A., Nance D. M., Cynader M. S. Laminar distribution of GABA-immunoreactive neurons and processes in area 18 of the cat. Brain Res Bull. 1987 Jan;18(1):121–126. doi: 10.1016/0361-9230(87)90040-2. [DOI] [PubMed] [Google Scholar]
  22. Matsubara J., Cynader M., Swindale N. V., Stryker M. P. Intrinsic projections within visual cortex: evidence for orientation-specific local connections. Proc Natl Acad Sci U S A. 1985 Feb;82(3):935–939. doi: 10.1073/pnas.82.3.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McCasland J. S., Woolsey T. A. New high-resolution 2-deoxyglucose method featuring double labeling and automated data collection. J Comp Neurol. 1988 Dec 22;278(4):543–554. doi: 10.1002/cne.902780406. [DOI] [PubMed] [Google Scholar]
  24. Shatz C. J., Stryker M. P. Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J Physiol. 1978 Aug;281:267–283. doi: 10.1113/jphysiol.1978.sp012421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Simons D. J., Carvell G. E. Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol. 1989 Feb;61(2):311–330. doi: 10.1152/jn.1989.61.2.311. [DOI] [PubMed] [Google Scholar]
  26. Simons D. J., Land P. W. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature. 1987 Apr 16;326(6114):694–697. doi: 10.1038/326694a0. [DOI] [PubMed] [Google Scholar]
  27. Simons D. J. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol. 1978 May;41(3):798–820. doi: 10.1152/jn.1978.41.3.798. [DOI] [PubMed] [Google Scholar]
  28. Simons D. J. Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol. 1985 Sep;54(3):615–635. doi: 10.1152/jn.1985.54.3.615. [DOI] [PubMed] [Google Scholar]
  29. Strominger R. N., Woolsey T. A. Templates for locating the whisker area in fresh flattened mouse and rat cortex. J Neurosci Methods. 1987 Dec;22(2):113–118. doi: 10.1016/0165-0270(87)90004-5. [DOI] [PubMed] [Google Scholar]
  30. Suga N., Tsuzuki K. Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat. J Neurophysiol. 1985 Apr;53(4):1109–1145. doi: 10.1152/jn.1985.53.4.1109. [DOI] [PubMed] [Google Scholar]
  31. Valverde F. Rate and extent of recovery from dark rearing in the visual cortex of the mouse. Brain Res. 1971 Oct 8;33(1):1–11. doi: 10.1016/0006-8993(71)90302-7. [DOI] [PubMed] [Google Scholar]
  32. Welker C., Woolsey T. A. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol. 1974 Dec 15;158(4):437–453. doi: 10.1002/cne.901580405. [DOI] [PubMed] [Google Scholar]
  33. White E. L., Keller A. Intrinsic circuitry involving the local axon collaterals of corticothalamic projection cells in mouse SmI cortex. J Comp Neurol. 1987 Aug 1;262(1):13–26. doi: 10.1002/cne.902620103. [DOI] [PubMed] [Google Scholar]
  34. Wiesel T. N. Postnatal development of the visual cortex and the influence of environment. Nature. 1982 Oct 14;299(5884):583–591. doi: 10.1038/299583a0. [DOI] [PubMed] [Google Scholar]
  35. Woolsey T. A., Van der Loos H. 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. 1970 Jan 20;17(2):205–242. doi: 10.1016/0006-8993(70)90079-x. [DOI] [PubMed] [Google Scholar]
  36. Woolsey T. A., Wann J. R. Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages. J Comp Neurol. 1976 Nov 1;170(1):53–66. doi: 10.1002/cne.901700105. [DOI] [PubMed] [Google Scholar]

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