Visual projections to the optic tecta in Xenopus after partial extirpation of the embryonic eye

The temporal, nasal or dorsal half (40–60%) of the eye primordium was excised in Xenopus frog embryos stage 25/26 (optic vesicle), 31/32 (optic cup) or 38 ± 1 (early larval eye). The residual nasal (NF) or temporal (TF) or ventral (VF) fragment gradually rounded‐up to form a grossly normal eye of normal or reduced size. Electrophysiologic analysis of the visuotectal projection after metamorphosis showed that (independent of stage of surgery and final eye size) most eyes of each type generated normal retinotectal maps (orderly and continuous retinotopic projection across the entire tectum). A minority of NF eyes generated double‐nasal compound maps, in which nasal and temporal halves of the adult retina projected as mirror images (of the nasal pattern) over the whole tectum. A minority of TF eyes generated double‐temporal compound maps, while a minority of VF eyes generated double‐ventral compound maps. Respectively, these compound maps simulated those generated by NN, TT or VV “compound‐eyes” prepared by fusing two nasal half eyes, or two temporal half eyes, or two ventral half eyes. The incidence of double‐maps was lowest in TF eyes at all stages, and after stage 25/26 surgery in all eye types. Lure tests and post‐synaptic recording confirmed that these eyes formed functional retinotectal synapses, and that the (presynaptic) map accurately mirrored the connectivity pattern. The results are considered in terms of (1) the patterning of locus specificities in the retinal ganglion cell population, (2) embryonic “regulation” and “reduplication” in non‐neural systems, and (3) alternative mechanisms by which partial extirpation might modify the deployment or expression of ganglion cell locus specificities to produce the retinotectal connectivity patterns we observed.

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

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

[3]  R. Hunt,et al.  The origins of nerve-cell specificity. , 1973, Scientific American.

[4]  Lewis Wolpert,et al.  Chapter 6 Positional Information and Pattern Formation , 1971 .

[5]  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 .

[6]  E. Hadorn Dynamics of Determination , 1966 .

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

[8]  R. G. Harrison,et al.  Experiments on the development of the fore limb of Amblystoma, a self‐differentiating equipotential system , 1918 .

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

[10]  A. Garcı́a-Bellido Pattern Formation in Imaginal Disks , 1972 .

[11]  R. Nöthiger The Larval Development of Imaginal Disks , 1972 .

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

[13]  H. Lüönd Untersuchungen zur Mustergliederung in fragmentierten Primordien des männlichen Geschlechtsapparates von Drosophila séguyi , 1961 .

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

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

[16]  R. Hunt,et al.  Patterning of neuronal locus specificities in retinal ganglion cells after partial extirpation of the embryonic eye , 1975 .

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

[18]  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.

[19]  L. Stone Polarization of the retina and development of vision , 1960 .

[20]  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.

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

[22]  M. Cynader,et al.  Receptive-field organization of monkey superior colliculus. , 1972, Journal of neurophysiology.

[23]  M. Cynader,et al.  Comparison of receptive‐field organization of the superior colliculus in Siamese and normal cats , 1972, The Journal of physiology.

[24]  Keating Mj The role of visual function in the patterning of binocular visual connexions. , 1974 .

[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]  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.

[27]  R. M. Gaze The formation of nerve connections , 1970 .

[28]  R. Sperry CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[29]  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.

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

[31]  W. B. Marks,et al.  Optic nerve terminal arborizations in the frog: shape and orientation inferred from electrophysiological measurements. , 1974, Experimental neurology.