M.P. Headon

Effects of monocular closure at different ages on deprived and undeprived cells in the primate lateral geniculate nucleus

This study has examined the effects of monocular visual deprivation on cells in the lateral geniculate nucleus of the primate by comparing the sizes of cells in deprived and undeprived LGN laminae of experimental rhesus monkeys with those of cells in the corresponding laminae of normal animals. A number of conclusions may be drawn from this comparison: monocular visual deprivation has major effects on cells in the undeprived LGN laminae and these vary with age at closure; the initial effect of monocular closure from birth is to cause marked hypertrophy of undeprived parvocellular cells with little shrinkage of the deprived parvocellular cells, whereas late monocular closure (after 2 months of age) causes marked shrinkage of both undeprived and deprived parvocellular cells; following monocular closure at birth, the LGN abnormality continues to evolve until at least 3 months of age, with a marked parallel shrinkage affecting both deprived and undeprived parvocellular cells. The initial hypertrophy of the undeprived cells is reversed and the deprived cells become smaller than normal; cells in the monkey LGN are sensitive to visual deprivation until about 1 year of age, much later than previously thought. Visual experience, however, modifies this sensitivity so that the effects of monocular visual deprivation are both qualitatively and quantitatively different at different ages; there are important differences between the susceptibility of cells in the magnocellular and parvocellular laminae to visual deprivation; and actual shrinkage of cells to markedly below normal size occurs and the smaller size is not simply failure of growth.

Effects of enucleation at different ages on the sizes of neurons in the lateral geniculate nucleus of infant and adult monkeys.

Cell areas have been measured in the lateral geniculate nucleus following enucleation in 7 infant and 3 adult monkeys. Deafferented cells showed rapid transneuronal degeneration. Following enucleation at birth non-deafferented parvocellular LGN cells underwent hypertrophy which was followed by a delayed return to normal size. Enucleation at 7 months of age caused marked shrinkage of non-deafferented parvocellular cells. These changes in the non-deafferented cells are similar to those following monocular lid closure at the same ages. Sizes of non-deafferented cells were unchanged following enucleation of adult monkeys.

Cell sizes in the lateral geniculate nucleus of normal infant and adult rhesus monkeys

Measurements of mean cell area have been made in the lateral geniculate nuclei of 16 normal rhesus monkeys as a control for changes following visual deprivation. There is little variability between animals and no significant growth between 8 days of age and adulthood in the parvocellular laminae. The magnocellular laminae show more variability and some continuing growth after 8 days of age.

Changes in the size of cells in the monocular segment of the primate lateral geniculate nucleus during normal development and following visual deprivation

Cell areas have been measured in the monocular segment of the lateral geniculate nucleus in a series of 18 normal rhesus monkeys and in 27 following monocular or binocular lid closure or monocular enucleation. Cells in the parvocellular monocular segment shrank by 16% during the later period of normal development, between about 3 and 18 months of age, in contrasts to cells in the binocular segment which did not. Monocular closure at birth caused hypertrophy of cells in the undeprived monocular segment whereas long-term closure started later caused shrinkage of both deprived and undeprived parvocellular cells additional to that occurring during normal development. In both these instances cells in the monocular segment related to the undeprived eye are undergoing changes indicating some form of binocular interactions even in the monocular segment, but these interactions are considerably weaker than in the binocular part of the nucleus. Enucleation caused marked transneuronal degeneration of cells in the contralateral monocular segment of both infant and adult monkeys.

Sizes of neurons in the primate lateral geniculate nucleus during normal development

Measurements of cell area have been made in the lateral geniculate nuclei (LGNs) of 18 normal rhesus monkeys aged from 8 days to fully adult. There is much less variability between individual animals than had been thought from measurements of undeprived cells in experimental animals following visual deprivation. It is therefore possible to make reliable comparisons of cell size between different animals. There is no change in size of cells in the parvocellular laminae between 8 days of age and adulthood, although cells in the magnocellular laminae grow a little. In the primate, unlike the cat, the period of maximum sensitivity to visual deprivation does not correspond to a period of rapid cell growth in the LGN.

Shrinkage of cells in undeprived laminae of the monkey lateral geniculate nucleus following late closure of one eye.

Comparisons of mean cell area in the lateral geniculate nucleus between normal and monocularly deprived rhesus monkeys show that late closure at between 3 months and a year of age produces up to 25% shrinkage of cells in the undeprived parvocellular laminae and up to 30% shrinkage in the deprived parvocellular laminae.

Simultaneous hypertrophy of cells related to each eye in the lateral geniculate nucleus of the infant monkey following short-term reverse suture.

Three infant monkeys were monocularly deprived from birth and reverse sutured at 3 weeks of age for a further period of 1, 2 or 5 weeks before perfusion. Cell areas were measured in the lateral geniculate nuclei and compared to those in normal monkeys and in monkeys following monocular closure. One week after reverse suture, cells in the initially deprived parvocellular laminae were 17% larger than normal and those in the initially undeprived laminae were 28% larger than normal. The initially undeprived parvocellular cells then shrank back to 14% larger than normal at 2 and 5 weeks while the initially deprived cells also remained hypertrophied. Following reverse suture at 3 weeks of age cells in parvocellular LGN laminae related to both eyes are simultaneously hypertrophied until at least 8 weeks of age and the LGN is therefore markedly abnormal even though the size difference between initially deprived and undeprived cells has been cancelled.

Initial hypertrophy of cells in undeprived laminar of the lateral geniculate nucleus of the monkey following early monocular visual deprivation

Comparisons of mean cell area in the lateral geniculate nucleus between normal and monocularly deprived Rhesus monkeys show that closure started in the first few days of life produces an initial hypertrophy of up to 25% affecting undeprived parvocellular cells. Hypertrophy is maximal at 4 weeks. Following this there is later shrinkage affecting both deprived and undeprived parvocellular cells so that ultimately undeprived parvocellular cells are about 10% smaller and deprived parvocellular cells about 35% smaller than corresponding cells in normal animals.

Experiments to study recovery of lateral geniculate nucleus cell size following monocular lid closure and reverse suture in infant monkeys

Following monocular eyelid closure at birth in macaque monkeys, reverse suture at 3 weeks of age cancels the difference in size between deprived and undeprived parvocellular lateral geniculate nucleus (LGN) cells by causing hypertrophy of the initially deprived cells. This means that two weeks after reversal cells in both initially deprived and initially undeprived parvocellular laminae are approximately 15% larger than normal. However, long term survival shows that there is a second phase of change during which all parvocellular cells shrink, but particularly the initially undeprived cells which become considerably smaller than the initially deprived cells. Reopening the secondarily closed eye after a short period of reversal resulted in normal cell sizes in one animal, but two animals developed marked squints and had very small parvocellular cells in all laminae, and one animal developed bilateral amblyopia. Simply reopening the eye of two animals after two months of late closure started at 7 months of age reversed the shrinkage of all parvocellular cells which is caused by late closure.

Effect of reopening an eye after a period of monocular deprivation on sizes of neurons in the primate lateral geniculate nucleus

Following monocular closure shortly after birth the deprived eye of 4 rhesus monkeys was reopened at different times. Following long-term recovery, cells in the undeprived laminae of the lateral geniculate nucleus of these animals were of normal size and those in the deprived laminae were markedly shrunken. Comparisons with animals monocularly deprived for similar periods indicate, however, that in 3 of these animals the undeprived parvocellular cells would have been markedly hypertrophied at the time of reopening the deprived eye, and in two of the animals, little shrinkage of the deprived parvocellular cells would have occurred by this time. Both undeprived and deprived parvocellular cells have therefore undergone marked shrinkage after the deprived eye had been reopened. The parallel shrinkage of deprived and undeprived parvocellular cells which occurs following closure at birth thus appears to be a consequence of the initial abnormalities produced by monocular closure rather than a direct result of the continuing lack of visual input to one eye.