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Segregation of Geniculocortical a Role for Subplate Neurons

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Segregation of Geniculocortical a Role for Subplate Neurons The Journal of Neuroscience, June 1994, 14(6): 38623880 Segregation of Geniculocortical Afferents during the Critical Period: A Role for Subplate Neurons Anirvan Ghosh and Carla J. ShatP Department of Neurobiology, Stanford University School of Medicine, Stanford, California 94305 To investigate the cellular interactions within the mammalian Visual experience can have a profound influence on the devel- visual cortex that are important in ocular dominance column opment of connections in the mammalian visual system. This formation, we have examined the role of subplate neurons phenomenonhas been most thoroughly investigated with regard in this process. LGN axons segregate in layer 4 of the cat’s to the system of ocular dominance columns in primary visual visual cortex between the third and sixth postnatal weeks cortex of cat and monkey (Hubel and Wiesel, 1977; LeVay et to give rise to the adult pattern of ocular dominance columns. al., 1980). Axon terminals from neurons of the lateral geniculate Subplate neurons are a transient population of neurons that nucleus (LGN), whose pattern of innervation of cortex gives sit in the white matter but have extensive projections into rise to ocular dominance columns, are initially intermixed with the overlying cortex, particularly layer 4, during neonatal life. regard to eye preference within layer 4 of visual cortex (Rakic, Many subplate neurons are present at birth, but most are 1976; LeVay et al., 1978). Events mediated by neuronal activity gone by the end of the period of LGN axon segregation. To and visual experience are known to be important in the for- examine whether these neurons are required for the seg- mation of ocular dominance columns in layer 4, since the final regation of LGN axons, we deleted them by intracortical in- pattern of ocular dominance is susceptibleto abnormal visual jections of kainic acid either just after LGN axons had grown experience during postnatal development. For example, in the into layer 4 (first postnatal week) or later, just before the cat, closure of one eye before segregationof LGN axons results onset of segregation (third postnatal week). The conse- in a large shift in ocular dominance in favor of the open eye quences for the patterning of geniculocortical terminals were (Wiesel and Hubel, 1963, 1965). Anatomical evidence indicates evaluated by transneuronal transport of 3H-proline injected that axon terminals driven by the open eye expand to occupy into one eye at times when segregation would normally be a larger area within layer 4, while there is a corresponding complete. Following deletion of subplate neurons at either shrinkage of the area representing the closed eye (Shatz and age, LGN axons failed to segregate into ocular dominance Stryker, 1978; LeVay et al., 1980). Experiments that interfere columns. Following the late deletions only, geniculocortical directly with action potentials or synaptic transmissionwithin axons lost their laminar restriction to layer 4 and projected cortex during postnatal development also prevent the anatom- to layers 2 and 3 as well. Deletion of subplate neurons also ical segregationof LGN axons within layer 4, suggestingthat resulted in long-term changes in the cytoarchitecture of activity and synaptic transmissionare necessaryfor LGN axons layer 4. to segregateunder normal circumstances(Stryker and Harris, These observations suggest that the interactions that me- 1986; Bear et al., 1990; reviewed in Shatz, 1990; Antonini and diate segregation of LGN axons within layer 4 of visual cortex Stryker, 1993). are susceptible to influences from subplate neurons. Al- The factors that permit activity-dependent change in axon though the mechanisms by which subplate neurons exert terminal arrangements are likely to have certain constraints, their effect are not yet clear, these experiments strongly since the anatomical pattern of ocular dominance columns in suggest that interactions between LGN axons and layer 4 layer 4 can be influenced by visual experience only during a neurons are not sufficient for column formation, and that restricted period in development- the critical period (Hubel and subplate neurons most likely play a critical role in interac- Wiesel, 1970; LeVay et al., 1980). A major question is, what tions leading to ocular segregation. changesoccur in the visual cortex that promote axonal segre- [Key words: subplate neurons, ocular dominance columns, gation and bring the critical period for layer 4 to a close?One visual system, geniculocortical axons, cortical plasticity, striking cellular change in the cortex that beginsjust before and critical period] concludesjust after LGN axon segregationis the disappearance ofsubplate neurons.These neuronssit directly below the cortical Received July 27, 1993; revised Dec. 3, 1993; accepted Dec. 2 I, 1993. plate and are presentin large numbersduring fetal development We thank members of the Shatz Lab for help with surgeries and Drs. E. I. (for reviews, see Shatz et al., 1991; Allendoerfer and Shatz, Knudsen, J. H. P. Skene, and W. T. Newsome for comments on the manuscript. 1993). In the cat, subplate neurons begin to disappear due to This work was supported by NIH Grant R37 EY02858 to C.J.S and a Bank of cell death a few days before birth-shortly after LGN axons America-Giannini Foundation postdoctoral fellowship to A.G. Correspondence should be addressed to Anirvan Ghosh, Department of Mi- grow into layer 4. Their numbers continue to decreaserapidly crobiology and Molecular Genetics, Harvard Medical School, 200 Longwood during the first month ofneonatal life, until the end ofthe second Avenue, DI-604, Boston, MA 02115. aPresent address: Division of Neurobiology, Department of Molecular and Cell postnatal month when most of them are gone (Valverde and Biology, LSA 221, University of California, Berkeley, CA 94720. Fatal-Valverde, 1988; Chun and Shatz, 1989b). Subplate neu- Copyright 0 1994 Society for Neuroscience 0270-6474/94/143862-19$05.00/O rons are important for earlier stepsin the development of LGN The Journal of Neuroscience, June 1994, f4(6) 3883 axons, and in fetal development apparently are required for Table 1. Age distribution of kainic acid-treated animals and method LGN axons to select visual cortex as an appropriate cortical of analysis target (Ghosh et al., 1990; Ghosh and Shatz, 1993). During neonatal cortical development, subplate neurons can have ex- Immuno- tensive axonal projections into layer 4 (Friauf et al., 1990), and histo- Num- Age at chemistry the neurons of layer 4 have a recurrent axon collateral within ber of kainic acid Aae at (MAP2. Autoradi- the subplate (Callaway and Katz, 1992) raising the possibility animals injection p&fusion GFAP) ogwhy that subplate neurons may influence events taking place in cor- 1 N/A P44 + tical layer 4. 1 P2 PlO + Here, we have investigated whether subplate neurons are in- 1 P3 P16 + volved in the process of ocular segregation of LGN axons in 2 P4 P18 + layer 4. LGN axons normally begin to segregate within layer 4 1 P5 P29 + beginning around the third postnatal week, and segregated oc- 1 P9 P31 + ular dominance columns can be seen clearly by the end of the 1 PI P14 + 3H-thy sixth week (LeVay et al., 1978). To examine the role of subplate 1 P7 P19 + 3H-thy neurons in segregation of the LGN axons, we deleted them by 1 P7 P20 ‘H-thy injecting small volumes of kainic acid into the white matter 1 P2 P70 )H-pro underlying visual cortex just prior to the onset of segregation 2 P2 P55 3H-pro and when they are still plentiful. At the end of the normal period 1 P2 P60 ‘H-pro of ocular segregation (6-8 weeks), we examined the pattern of 2 P3 P47 ‘H-pro ocular dominance columns in layer 4 of the subplate-ablated 1 P4 P48 ‘H-pro hemisphere by means of transneuronal transport of 3H-proline 1 P5 PlOO 3H-pro (Wiesel et al., 1974a; Shatz et al., 1977). We found that in the 2 P6 P55 ‘H-pro absence of subplate neurons the segregation of LGN axons into 1 P& P55 3H-pro ocular dominance columns fails to take place. In addition, the 1 PP P60 ‘H-pro deletion of subplate neurons alters the cytoarchitectural .orga- 1 PllO P62 ‘H-pro nization of visual cortex, particularly within cortical layer 4. 2 P18 P50 )H-pro Materials and Methods 2 P20 P46 )H-pro Cortical injections of kainic acid were made in 26 cats between postnatal ‘H-thy, autoradiography following intrauterine injections of fH-thymidine at E39 day 2 (P2) and P20, and the consequences examined between P14 and or E40 to label layer 4 cells. ‘H-pro, autoradiography following intraocular injec- PlOO. The pattern of labeling of geniculocortical axon terminals was tions of ‘H-proline into the eye ipsilateral to kainic acid-injected hemisphere. visualized by an intraocular injection of 3H-proline into the eye ipsi- a In these animals kainic acid was injected directly into the cortical plate. In all other experiments kainic acid was injected into the white matter underlying visual lateral to the kainic injection 1 week prior to perfusion. The fate of layer cortex. 4 neurons in experimental animals was evaluated by labeling layer 4 cells in utero with an injection of 3H-thymidine at E39 or E40 and, subsequently, examining the distribution ofthe labeled cells in subplate- slides. Air-dried sections were dehydrated in graded alcohols, defatted ablated animals. Several animals were also processed for histology and in xylenes,and coverslipped. immunocytochemistry to evaluate the effects of the kainic acid lesions Autoradioaraohv. One week to 10 d following. eve iniection of )H- on the cytoarchitecture of visual cortex. The distribution of ages ex- proline the &imals were perfused with 4% paraformaldehyde in 0.1 M amined and the various analytical procedures are summarized in Ta- sodium phosphate buffer. The brain was removed and postfixed in the ble 1.
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