Absence of Adaptive Modification in Developing Retinotectal Connections
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1 Proceedings of the National Academy of Sciences Vol. 68, No. 3, pp , March 1971 Absence of Adaptive Modification in Developing Retinotectal Connections in Frogs after Visual Deprivation or Disparate Stimulation of the Eyes MARCUS JACOBSON Biophysics Department, Johns Hopkins University, Baltimore, Maryland Communicated by Martin G. Larrabee, December 21, 1970 I;,- " ABSTRACT Action potentials evoked in the tectum by visual stimulation of the ipsilateral eye were absent in frog larvae and developed during metamorphosis. Formation of the connections underlying these responses is not based on the animal's visual experience. The development of the ipsilateral retinotectal projection occurred normally in frogs reared through metamorphosis in the dark from midlarval stages to adults. Inversion of one eye of frog larvae did not affect the development of ipsilateral retinotectal projections, which developed according to the inherent correspondences between the retinae regardless of the disparities produced by changing the relative positions of the eyes. No compensatory changes occurred in the retinotectal projections in response to the surgical derangement. Skin grafts completely occluding one eye, which were made at early larval stages and left in place for up to 88 days, did not affect the development of normal ipsilateral retinotectal connections. However, abnormal ipsilateral tectal responses evoked by stimulation through either the normal eye or the occluded eye were found in adult frogs after occlusion of one eye from larval stages for more than 121 days. It was concluded that visual stimulation is not required for the normal development of ipsilateral retinotectal connections but is required for their long-term maintenance. This paper is a critical examination of the hypothesis proposed recently by Gaze, Keating, Szekely, and Beazley that the development of neuronal connections subserving binocular vision in amphibians is contingent upon visual experience (1). They observed that the ipsilateral retinotectal projection from one eye corresponded with the contralateral projection from the other eye in Xenopus reared from embryonic stages with one eye inverted or with one compound eye constructed from two identical half eyes. Thus, the projection from the normal eye to the ipsilateral tectum was abnormal, but in correspondence with the projection to that same tectum from the deranged eye. The projection from the deranged eye to its ipsilateral tectum was modified so that it was in correspondence with the projection to that tectum from the normal eye. To account for these findings, they suggested that since each point in the binocular visual field excites corresponding points in the two retinae, the resulting simultaneous excitation of fibers from the two eyes would result in a selective linkage of the appropriate ipsilateral and contralateral nerve fibers. This is called the binocular functional interaction hypothesis. It should be emphasized that tadpoles have no binocular visual field so that visual stimulation cannot play a role in the development of binocular retinotectal connections until metamorphosis. At that time, the eyes move to a more frontal position and the visual fields of the two eyes overlap. While it 528 is known that the contralateral retinotectal projection develops in the embryo (2, 3), it is not kno*n when the ipsilateral projection develops. Both projections have been mapped electrophysiologically in adult frogs (4, 5). The aim of this investigation was to test the binocular functional interaction hypothesis in several ways. The hypothesis requires that the ipsilateral retinotectal projection, which subserves binocular vision in the frog, should only develop during or after metamorphosis, and that the ipsilateral projection would not develop normally in animals reared in the dark, or reared with monocular visual occlusion. The functional interaction hypothesis also predicts that inversion of one eye would result in compensatory changes in the ipsilateral retinotectal projection of frogs reared through metamorphosis without visual restriction, as the originators of the hypothesis found in Xenopus (1). To test the hypothesis, I mapped the retinotectal projections electrophysiologically in adult and metamorphosing frogs that had been reared normally and compared them with the retinotectal projections in frogs that had been reared from midlarval stages in complete darkness. Comparisons were also made with retinotectal projections in normal frogs and in other frogs that had been reared from early larval stages with a skin graft completely occluding one eye, or with one eye inverted. The effects of different durations of disparity between the eyes was also studied. METHODS All experiments were on Rana pipiens reared from eggs and staged according to the normal table of Taylor and Kollros (6). Retinotectal projections were mapped in 41 tadpoles and frogs in the following four experimental groups (Table 1): N Group, consisting of fourteen normal tadpoles at larval stages XVII- XIX and metamorphic stages XX-XXV to determine the time of development of ipsilateral retinotectal projections; D group, consisting of twelve young adult frogs that had been reared from larval stages in the dark; SG Group, consisting of nine adult frogs that had one eye completely occluded by skin grafts from the back that remained continuously in place from different larval stages (Table 1). The occluded eye developed normally and the graft could be removed, without damaging the eye, immediately before mapping the retinotectal projections. EI Group, consisting of six adult frogs that had been reared from larval stages with one eye dorsoventrally inverted. In two of these (EI-1 and E14) the optic nerve was transected, and in four (EI-2, 3, 5, and 6) the optic nerve was left intact from the time of eye inversion.
2 Proc. Nat. Acad. Sci. USA 68 (1971) Mapping technique After anesthesia in an aqueous solution of tricaine methane sulphonate (1:2000) and paralysis with 0.01 mg of tubocurarine injected intramuscularly, the dorsal surface of the tectum was exposed. The frog was fixed with the right eye centered on a perimeter on which spots of light or black discs of diameters subtending 10' to 50 could be positioned. These stimuli evoked action potentials in the tectum that were recorded with a tungsten microelectrode (tip diameter about 2 gm). Action potentials were sometimes recorded from a single unit, but were usually from several units firing simultaneously in the superficial layers of the tectum. The electrode position was moved systematically in 250-,um steps across the tectum; at each location the receptive field position was determined independently through each eye, the other being covered by a black contact lens. In normal frogs, at each electrode position, responses could be evoked from a receptive field 5-10 in diameter. RESULTS These are summarized in Table 1. N Group. No ipsilateral responses were detected in stage XVII and XVIII larvae, although contralateral responses were normal. Ipsilateral responses were first detected at stage XIX. At this stage, the ipsilateral projection was retinotopically organized in the normal way except that the multiunit receptive fields were much larger than in the adult; they ranged from 250 to 50 in diameter. Receptive fields were slightly smaller (20-30 ) at stages XX-XXIII, and were about in diameter at stages XXIV and XXV. Starting at stage XIX, there was a normal correspondence between ipsilateral and contralateral projections to the tectum. That is, at any electrode position on the tectum that gave responses through the ipsilateral eye, responses were evoked from the same position in the visual field through the contralateral eye. D Group. Animals kept in the dark from larval stage XVII through metamorphosis developed normal ipsilateral visual projections. This demonstrates that ipsilateral retinotectal projections develop in the absence of any visual stimulation. SG Group. Excluding patterned visual stimulation from one eye by covering it with a skin graft from early larval stages to adulthood (up to 88 days) did not prevent the development of normal ipsilateral retinotectal responses and projections. By recording first with the skin graft still in place, it was shown that small stationary or moving black discs, as well as spots of light, could evoke neither contralateral nor ipsilateral responses through the graft. The only normal tectal responses recorded by stimulation through the graft were from units that were activated by changes in overall illumination. After removal of the grafts, however, normal responses were obtained from all classes of tectal units that responded to small stationary or moving stimuli (7). The results demonstrate thajt although the graft had effectively prevented patterned stimulation of one eye, the ipsilateral retinotectal projection developed normally despite asymmetrical inputs from the two eyes (Fig. 1). Whereas short-term deprivation of patterned visual stimulation for days had no effect, long-term monocular occlusion of one eye from larval stages for days resulted in significant abnormalities in the ipsilateral tectal responses evoked TABLE 1. Results of mapping retinotectal projections in four groups of frogs Days between Larval Larval operation stage at stage at and Resulting Expt. operation mapping mapping pattern N-1 and N-2 - XVII No responses N-3 XVIII No responses N-4 XIX - A N-5 XX A N-6 and N-7 XXI - A N-8 and N-9 XXII A N-10 XXIII A N-11 and N-12 - XXIV Normal N-13 and N-14 - XXV Normal D-1 and D-2 XVII Adult 36 Normal D-3 and D-4 XVIII Adult 34 Normal D-5 and D-6 XIX Adult 22 and 41 Normal D-7 and D-8 XX Adult 27 and 38 Normal D-9 and D-10 XXI Adult 37 and 52 Normal D-ll and D-12 XXII Adult 22 Normal D-13 and D-14 XXIII Adult 30 Normal SG-1 II Adult 64 Normal SG-2 III Adult 167 B SG-3 XIV Adult 50 Normal SG-4 XIV Adult 62 Normal SG-5 XVI XXV 16 Normal SG-6 XVI Adult 67 Normal SG-7 XVI Adult 183 B SG-8 XX Adult 121 B SG-9 XXI Adult 88 Normal EI-1 IX Adult 154 C EI-2 XIX Adult 173 C EI-3 XX Adult 17 D EI-4 XXI Adult 100 C EI-5 XXIII Adult 20 D EI-6 XXIII Adult 33 D All contralateral projections were normal. Ipsilateral projections were either normal or altered according to one of the following patterns for both eyes: A: Large ipsilateral receptive fields but normal retinotopic pattern. B: Large ipsilateral receptive fields. Normal correspondence between left- and right-eye fields recorded at same tectal position. C: As in B, but with noncorrespondence between left- and righteye receptive fields. D: Normal ipsilateral responses and receptive fields but noncorrespondence between left- and right-eye receptive fields recorded at the same tectal position. through either eye. The contralateral responses were normal in these cases. The abnormalities consisted of reduction in the amplitude of tectal action potentials evoked through the ipsilateral eye. Action potentials were reduced from the normal range of ,V to less than 100,uV. In addition, the multiunit receptive fields of ipsilateral responses were greatly increased in size; responses could be evoked from an area of the visual field subtending Abnormal ipsilateral tectal responses were evoked through the normal eye as well as through the previously occluded eye. Develo ment of Frog Eye 529
3 530 Zoology: M. Jacobson Proc. Nat. Acad. Sci. USA 68 (1971) T 3 1T9 N VISUAL FIELD VISUAL FIELD / RIGHT TECTUM v \ / ~~TECTUM / V ~~~~~~~ i 38 \ RIGHT EYE LF Y I FIG. 1. Normal visual field projections through both eyes to the ipsilateral and contralateral tectum in an adult frog (SG-3) that had developed from larval stage XIV with a skin graft occluding the left eye. All four visual field maps should be superimposed, and represent the visual field of both eyes, mapped with the right eye centered. Each number in the visual field shows the position of the stimulus that optimally evoked potentials recorded by an electrode at the position shown by the same number on the tectum. Tectal electrode positions were spaced 250-,um apart. The visual field extends 1000 from the center to the periphery. I EI Group. In all cases the angular disparity in the positions of the eyes was exactly matched by the disparity between the ipsilateral and contralateral projections (Fig. 2). Despite disparate stimulation through the two eyes during and after metamorphosis, no adaptation of the projections had occurred. Normal evoked potential responses and receptive fields were recorded in frogs with monocular eye inversion that had only survived a short period after passing through metamorphosis with the visual disparity (Table 1), but long-term disparity between the eyes, lasting days, resulted in abnormalities in the ipsilateral retinotectal responses. These abnormalities were similar to those found after monocular occlusion with a skin graft, but were not as marked in the frogs with inverted eyes as in those with skin grafts over one eye. Abnormally large receptive fields and low voltage, evoked action potentials were recorded equally in the ipsilateral tectum whichever eye was stimulated, although the responses in the contralateral tectum were normal. DISCUSSION Action potentials in the tectum indicating the presence of ipsilateral retinotectal connections can first be recorded at larval stage XIX, and show evidence of further development during subsequent metamorphic stages XX-XXV. As early as stages XIX-XX, there is clear evidence of retinotopic arrangements of the ipsilateral retinotectal projection and of correspondence between ipsilateral and contralateral projections. Since these projections are normal in frogs reared in darkness from larval stage XVII through metamorphosis, visual stimulation is not required for their initial development. Symmetrical deprivation (or stimulation) of the two eyes cannot test the hypothesis that simultaneous activation of
4 Proc. Nat. Acad. Sci. USA 68 (1971) Development of Frog Eye 531 S S FIG. 2. Visual field projections through both eyes to the tectum in adult frog (EI-1) that had developed from larval stage IX with the right eye inverted without cutting the optic nerve. The conventions are the same as in Fig. 1. fibers from the two eyes results in the establishment of selective links between the appropriate ipsilateral and contralateral fibers. For this reason, experiments that produce disparities between the eyes must be used in any critical test of this hypothesis. When patterned stimulation was excluded from one eye by a skin graft, from larval to adult stages, ipsilateral projections developed normally despite the tremendous difference that has been demonstrated in the activation of tectal units of different functional types by the two eyes. Even more significantly, in frogs reared with unilateral eye inversion, corresponding points on the two retinae received different patterns of stimulation, and yet retinotectal projections linking corresponding retinal points to the same point on the tectum developed normally. This evidence is inconsistent with the hypothesis proposed by Gaze, Keating, Sz6kely, and Beazley (1). Their model implies that when one eye is inverted, fibers from points in the two eyes that are stimulated by one locus in visual space will be selectively linked together in the tectum because they simultaneously receive the same pattern of excitation during and after metamorphosis. However, as Fig. 2 shows, no tectal linkages were established between points on the two retinae that were brought into functional correspondence after inversion of one eye. Rather, tectal linkages developed between retinal points that were intrinsically in correspondence in the normal, nonrotated, position of the eyes. This evidence leads to the conclusion that the initial development of ipsilateral retinotectal projections is intrinsically determined by genetic and developmental mechanisms. Similar conclusions have already been reached about the mechanism of development of contralateral retinotectal projections (8). The experiments of Hubel and Wiesel (9, 10) on the effects of visual deprivation in kittens appear to be most relevant to these experiments on frogs. However, comparisons are limited by differences in the species studied and in the techniques used. Hubel and Wiesel showed that at birth the kitten's visual cortex contains single units that could be driven by either eye,
5 532 Zoology: M. Jacobson but these binocularly driven units disappeared if the kitten was prevented from using both eyes together for a critical period between the fourth and sixth weeks after birth. Because my experiments on the frog employed multiunit recording, the effects of visual deprivation on binocularly driven tectal units were not studied. These results, however, suggest that the ipsilateral projections do differ from the contralateral ones in being adversely affected by long periods of monocular eye inversion or occlusion. These disparities between the eyes resulted, after several months, in increased size of visual receptive fields projecting to the ipsilateral tectum from the normal eye as well as from the deranged eye. These abnormalities of the ipsilateral retinotectal projections cannot be simply the result of visual deprivation because inversion of one eye, without section of the optic nerve, did not result in a reduction of patterned visual stimulation or of the total quantity of visual stimulation. Rather, asymmetrical stimulation of the two eyes appears to be the significant factor, both after inversion or occlusion of one eye. This would help to explain why the ipsilateral responses from both the normal and the inverted or occluded eye were affected. We may postulate that some kind of functional interaction between Proc. Nat. Acad. Sci. USA 68 (1971) the fibers that converge to one position on the tectum from corresponding points on the ipsilateral and contralateral eyes is required for the maintenance of ipsilateral retinotectal connections. However, visual function is not concerned in the initial development of those connections. I thank Dr. H. V. B. Hirsch for assistance with some of the experiments and for a critical reading of the manuscript. This work was supported by grant GB 24900X from the National Science Foundation. 1. Gaze, R. M., M. J. Keating, G. Szekely, and L. Beazley, Proc. Roy. Soc. (London), Ser. B., 175, 107 (1970). 2. Sperry, R. W., Proc. Nat. Acad. Sci. USA, 50, 703 (1963). 3. Jacobson, M., Develop. Bil., 17, 202 (1968). 4. Gaze, R. M., and M. Jacobson, Quart. J. Exp. Phyeiol., 47, 273 (1962). 5. Jacobson, M., Quart. J. Exp. Physiol., 47, 170 (1962). 6. Taylor, A. C., and J. J. Kollros, Anat. Rec., 94, 7 (1946). 7. Maturana, H. R., J. Y. Lettvin, W. S. McCulloch, and W. H. Pitts, J. Gen. Physiol. Suppl., 43, 129 (1960). 8. Sperry, R. W., Growth Symp., 10, 63 (1951). 9. Hubel, D. H., and T. N. Wiesel, J. Neurophysiol., 28, 1041 (1965). 10. Hubel, D. M., and T. N. Wiesel, J. Physiol. (London), 206, 419 (1970).
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