Patterning of neuronal locus specificities in retinal ganglion cells after partial extirpation of the embryonic eye

A variety of transplantation procedures were used to analyze the determinants of locus specificity pattern in eye fragments prepared at stage 31/32. When right eye fragments were rotated through 0–360° in situ, or grafted to a stage 31/32 or stage 27/28 host, or grown in vitro 48 hours prior to reimplantation, the orientation of the retinotectal map always matched the anatomical orientation of the rounded‐up fragment, while the internal organization of the map was characteristic for the original fragment type: normal or double‐nasal in NF eye grafts, normal or double‐temporal in TF eye grafts, normal or double‐ventral in VF eye grafts. Fragments from stage 31/32 left eyes showed similar behavior, but mapped from the right orbit with one axis inverted as occurs after contralateral transplantation of whole left eyes. When one rounded‐up fragment and one normal eye (or one rounded‐up nasal fragment and one rounded‐up temporal fragment) were placed side‐by‐side in the same orbit and allowed to “superinnervate” the same tectum, both retinae mapped across the entire tectum with no unshared tectal regions. Finally, in fragments prepared from previously‐rotated (at stage 25/26) eyes, the organization and orientation of the map conformed to the new retinal axes, often in direct conflict with the anatomical polarity of the eye. The results are considered in terms of (1) the histogenesis of the retina in eye fragments; (2) the stability of the program for patterning of locus specificities, which is set down when the optic cup undergoes axial specification at stages 28–31; (3) the factors controlling selective modification of this program and their localization in eye fragments; and (4) the extent to which the range of locus specificities, deployed across the ganglion cell population of rounded‐up fragments, approximates that found in the normal unoperated eye.

[1]  J. Hollyfield,et al.  Specification of retinal central connections in Rana pipiens before the appearance of the first post‐mitotic ganglion cells , 1974, The Journal of comparative neurology.

[2]  M. Jacobson Cessation of DNA synthesis in retinal ganglion cells correlated with the time of specification of their central conections. , 1968, Developmental biology.

[3]  W. Cowan,et al.  The specification of the retino‐tectal projection in the chick , 1974, The Journal of comparative neurology.

[4]  R. Hunt,et al.  Neuronal Locus Specificity: Altered Pattern of Spatial Deployment in Fused Fragments of Embryonic Xenopus Eyes , 1973, Science.

[5]  W. Sturtridge,et al.  The physiological role of calcitonin assessed through chronic calcitonin deficiency in rats , 1973, The Journal of physiology.

[6]  R. M. Gaze,et al.  The Visual System and “Neuronal Specificity” , 1972, Nature.

[7]  R K Hunt,et al.  Specification of positional information in retinal ganglion cells of Xenopus: stability of the specified state. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Hunt,et al.  Development and stability of postional information in Xenopus retinal ganglion cells. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Hunt,et al.  Development of neuronal locus specificity in Xenopus retinal ganglion cells after surgical eye transection after fusion of whole eyes. , 1974, Developmental biology.

[10]  R. Sperry,et al.  Tests for neuroplasticity in the anuran retinotectal system. , 1973, Experimental neurology.

[11]  R. M. Gaze,et al.  On the formation of connexions by compound eyes in Xenopus , 1965, The Journal of physiology.

[12]  R. M. Gaze,et al.  The development of half‐eyes in Xenopus tadpoles , 1975 .

[13]  P. Bryant Determination and pattern formation in the imaginal discs of Drosophila. , 1974, Current topics in developmental biology.

[14]  J. Abbott,et al.  Oscillations of the Chondrogenic Phenotype in vitro , 1968 .

[15]  M. Yoon Transposition of the visual projection from the nasal hemiretina onto the foreign rostral zone of the optic tectum in goldfish. , 1972, Experimental neurology.

[16]  R. Hunt The Cell Cycle, Cell Lineage, and Neuronal Specificity , 1975 .

[17]  R. M. Gaze,et al.  The retino‐tectal projection in Xenopus with compound eyes , 1963, The Journal of physiology.

[18]  R. Hunt,et al.  Visual projections to the optic tecta in Xenopus after partial extirpation of the embryonic eye , 1975 .

[19]  M. Jacobson Development of neuronal specificity in retinal ganglion cells of Xenopus. , 1968, Developmental biology.

[20]  R. Hunt,et al.  Chapter 7 Neuronal Specificity Revisited , 1974 .

[21]  J. Hollyfield Differential growth of the neural retina in Xenopus laevis larvae. , 1971, Developmental biology.

[22]  J. Faber,et al.  Normal table of Xenopus laevis (Daudin). A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. , 1956 .

[23]  R. M. Gaze,et al.  The evolution of the retinotectal map during development in Xenopus , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[24]  R. Hunt,et al.  Specification of positional information in retinal ganglion cells of Xenopus laevis: intra-ocular control of the time of specification. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Hunt,et al.  Specification of positional information in retinal ganglion cells of Xenopus: assays for analysis of the unspecified state. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Cook,et al.  Proceedings: Interactions between optic fibres in their regeneration to specific sites in the goldfish tectum. , 1974, The Journal of physiology.

[27]  J. Whittaker The Nature and Probable Cause of Modulations in Pigment Cell Cultures , 1968 .

[28]  R. G. Harrison,et al.  On relations of symmetry in transplanted limbs , 1921 .