Effects of Early Unilateral Blur on the Macaque's Visual System. II
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The Journal of Neuroscience, May 1987, 7(5): 1327-l 339 Effects of Early Unilateral Blur on the Macaque’s Visual System. II. Anatomical Observations Anita E. Hendrickson,lB2 J. Anthony Movshon, 4 Howard M. Eggers,5 Martin S. Gizzi,4,a Ronald G. Boothe,3,b and Lynne Kiorpes3zc Departments of ‘Biological Structure, 20phthalmology, and 3Psychology, University of Washington, Seattle, Washington 98195; 4Department of Psychology, New York University, New York, New York 10003; and 5Harkness Eye Institute, College of Physicians and Surgeons, Columbia University, New York, New York 10036 We studied the effects of early unilateral blur on the ana- natal blur preferentially affects the parvocellular layers of tomical organization of the visual pathways in 8 macaque the LGN and layer 4Cfl of striate cortex, which are the por- monkeys. Blur was induced in one eye, beginning 2-14 d af- tions of the central visual system associated with the pro- ter birth, by 0.5% atropine twice a day. Atropiniration was cessing of information concerning fine spatial detail. These stopped at 6-8 months of age, and the animals were studied anatomical changes are consistent with the high spatial fre- for anatomy 3-24 months later. The retina and all other eye quency loss of vision demonstrated behaviorally and elec- tissues showed normal histology. In the dorsal lateral ge- trophysiologically in the atropine eye-driven visual system niculate nucleus (LGN), cells in parvocellular layers receiv- of these same animals. ing input from the atropine-treated eye were 9-32% smaller and were more lightly stained than those in layers innervated Amblyopia is a lossof visual function that is not due to optical by the untreated eye. These changes were generally larger abnormalities or peripheral pathology. The visual lossesseen in the LGN ipsilateral to the treated eye. LGN cell size changes in monocularly lid-sutured monkeys representthis condition in were absent or much smaller in the magnocellular layers. In a particularly severe form. Among the most striking changes the striate cortex, the distribution of the oxidative enzyme that occur in the primate visual system following early eyelid cytochrome oxidase (CO) was markedly altered in layer 4C@. suture are anatomical alterations in the dorsal lateral geniculate Layer 4Ca is uniformly stained in normal animals, but showed nucleus(LGN) and striate cortex. Cell size and basophilic stain- a distinct pattern of alternating high and low CO bands in ing are markedly reduced in all LGN layers containing ganglion the atropine-treated animals; the bands of higher CO activity cell terminals from the retina of the deprived eye (von Noorden were narrower than the bands of lower activity and had a et al., 1970; von Noorden and Middleditch, 1975b; Hubel et 857-l 050 pm repeat. Fainter banding was seen in layers 4A, al., 1977; GareyandVital-Durand, 1981; Headon et al., 1985b). 4Ca, and 6, but the density of the rows of dark CO-stained When the projections of LGN cells are studied, their axon dis- dots in layer 3 was unaffected. Double-labeling revealed that tribution in striate cortex is seen to be contracted, while the the narrow dark CO bands were associated with the centers axons from cells in LGN layers driven by the normal eye are of the ocular dominance columns devoted to the atropine- expanded in a complementaryfashion (Hubel et al., 1977; LeVay treated eye. The distribution of 14C-2-deoxyglucose uptake et al., 1980; Swindale et al., 198 1). Bands of LGN input in in visual cortex produced by 4.5-9 cldeg spatial frequency striate layer 4C are the anatomical representation of the ocular stimulation was strongly biased toward the untreated eye. dominance columns (Hubel and Wiesel, 1968), each of which The treated eye could, however, elicit reasonably strong is 350-500 pm wide in a normal monkey (Hubel and Wiesel, uptake when stimulated with patterns containing lower spa- 1972; Hendrickson et al., 1978). In a lid-sutured monkey, the tial frequencies. These results suggest that unilateral neo- open eye expands its territory so that its axons occupy 60-90% of layer 4C; closureswithin the first week after birth causelarger Received Apr. 21, 1986; revised Dec. 5, 1986; accepted Dec. 5, 1986. changesthan closuresat 8- 10 weeks, near the end of the critical This research was supported by NIH Grants EY01208, EY04536, EY01730, period (Hubel et al., 1977; LeVay et al., 1980; Swindale et al., EY02017, EY02536, RRO0166, and HD02274. A.E.H. is the recipient ofa Dolly 1981). This change in LGN synaptic input within layer 4C is Green Scholar Award from Research to Prevent Blindness, Inc. J.A.M. held g Research Career Development Award from NIH (EYO0187). M.S.G. was partly accompanied by a loss of functional connections from the lid- supported by a grant from the New York State Health Research Council. We are sutured eye throughout the visual cortex (Hubel et al., 1977; grateful for the critical suggestions of Dr. Helen Sherk, the excellent technical LeVay et al., 1980; Blakemore et al., 1981) and also by a pro- assistance of Bente Noble, Bradley Clifton, Ronald Jones, and Mark Hartley, and for the cooperation of United Airlines. found behavioral loss of vision in this eye (von Noorden et al., Correspondence should be addressed to Dr. J. A. Movshon, Department of 1970; von Noorden, 1973; Hendrickson et al., 1977; Harwerth Psychology, New York University, 6 Washington Place, New York, NY 10003. et al., 1981). = Present address: Department of Neurology, Mount Sinai Medical School, New York, NY 10036. In humans, amblyopia is often causedby early visual expe- b Present address: Department of Psychology, Emory University, Atlanta, GA rience with a blurred retinal image in one eye due to refractive 30322. c Present address: Department of Psychology, New York University, New York, imbalance (anisometropia). This situation is not as drastic in NY 10003. its visual effects as lid suture in monkeys, although rare occur- Copyright 0 1987 Society for Neuroscience 0270-6474/87/051327-13$02.00/O rencesof total lid closurein human infants (von Noorden, 1973) 1328 Hendrickson et al. - Anatomical Effects of Early Unilateral Blur Table 1. Summary of the rearing conditions and behavioral testing results from 8 monkeysa Monkey Characteristic LD TC DH NW GO GZ OH OL Rearing history Eye treated R L R L L R R R Atropine begun (d) 14 10 5 10 6 13 14 2 Atropine ended (mo.) I 8 10 8 6 7 6 6 Sacrificed (mo.) 30 25 22 13 9 10 12 14 Final refraction Untreated eye +1.50 +3.25 0 +2.00 - +1.00 - + 1.50 Treated eye +2.15 +3.25 +6.00 +5.00 - +2.50 - +3.50 Behavioral and evoked potential measurements, final acuity (cycles/deg) Untreated eye 34.9 31.5 36.9 29.6 51.5b.C 43 19.36 22.8’ Treated eye 29.3 28.1 3.7 6.7 18.7c 4.2 13.36 5.3 y See previous paper (Kiorpes et al., 1987) for further details. h High-frequency portion of function poorly defined. c Evoked potential measurements only. or prolonged therapeutic monocular patching (Awaya et al., of the retinal image, while the signalspassing through the mag- 1973; Levi and Harwerth, 1980) show that the neonatal human nocellular layer (the “M” system)emphasize information about visual system is at least as sensitive to monocular occlusion as lower contrast spatial features and the temporal content of the that of the monkey. We wished to study a deprivation paradigm retinal image (Schiller and Malpeli, 1978; Kaplan and Shapley, more akin to the unequal refractive error common in humans 1982; Derrington and Lennie, 1984; but seediffering views of and so choseto treat one eye of neonatal monkeyswith atropine. Shapley and Perry, 1986). In the first paper of this series(Kiorpes Atropinization produces a blurred retinal image by paralyzing et al., 1987), we showed that the visual behavioral defects in the pupillary constrictor muscle to keep the pupil in the fully atropine-treated monkeys are primarily confined to high spatial dilated state and the ciliary muscle to prevent lens accommo- frequencies. It is therefore natural to speculatethat the effects dation for near vision. This producesa lossof image sharpness of early blur might be more pronounced in the P than the M comparable in magnitude to that which leads to amblyopia in system. In this paper, we describe anatomical changesin the humans.In support of this assertion,we previously have shown visual pathways of these samemonkeys that suggestthis to be that atropinization produces an amblyopia-like visual behav- the case. The final paper of this series(Movshon et al., 1987) ioral deficit in monkeys (Boothe et al., 1982; Kiorpes et al., shows that the effects of this rearing on the functional charac- 1987). teristics of visual cortical neurons are also consistent with a By applying modem neuroanatomical techniquesto the visual selective effect on visual mechanismsresponsible for the relay system of these same animals, we hoped to ascertain whether of high spatial frequencies. there were selective changesin any of its subdivisions. This was motivated by the view that the macaque’svisual systemcontains Materials and Methods 2 major “functional streams” of visual information processing, Subjects. The monkeys used in these experiments were the 8 macaques which originate in 2 classesof retinal ganglion cells, Pot and P@ (Mucaca nemestrina) whose rearing and treatment are described in the (Hubel and Weisel, 1972; Schiller and Malpeli, 1978; Lund, preceding paper (Kiorpes et al., 1987). The retinal image of one eye of 1980). Pp cells project to the parvocellular layers of the LGN, each animal was blurred by twice-daily instillation of 0.5% atropine from 2-14 d after birth to at least 6 months of age.