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eye. It seems that, although changes associated with monocular deprivation have been found at the level of retino-geniculate terminals, in the LGN cell bodies, in the LGN terminal and in cortical cells’ responses, the primary site of binocular competition is cortical, and other changes in the visual system are secondary to the primary cortical competition.
This change in ocular dominance, as in all major rewiring in the visual system, occurs during a limited period following birth, often called the critical or sensitive period. It seems that the visual system is only capable of rewiring itself in this small temporal window and can do very little more once this opportunity has elapsed. For kittens, deprivation for only 3 days between the fourth and fifth week causes a large change in the pattern of ocular dominance (Hubel & Wiesel, 1970). If deprivation was started later than the eighth week, similar effects were observed, until even long periods of deprivation at four months caused no effect (Figure 6.4). Hubel and Wiesel concluded that the critical period for susceptibility to monocular deprivation begins in the fourth week and extends to about 4 months of age. Deprivation does not have to be long to cause large effects if it occurs during the critical period. Occluding one of the eyes of a 4-week-old kitten for a single day causes a large effect on the pattern of ocular dominance (Olson & Freeman, 1975) (Figure 6.5). However, it seems that the critical period is not fixed (Cynader, 1983). If cats are reared in the dark until long after the end of the chronologically defined critical period and only then brought into the light for monocular deprivation, this deprivation can still produce marked effects on cortical ocular dominance. Dark-reared cats seem to undergo a new critical period in the first few weeks after they are brought into the light. So, not only is the rewiring activity dependent but so is its initiation.
A similar situation to that described above in non-human mammals for monocular deprivation may also occur in human subjects. There is increasing evidence that amblyopia (a large reduction in the visual acuity in one eye) may sometimes occur in humans who, as young children, had the reduced use of one eye because of patching following an eye operation. This evidence has been provided by investigating the histories of 19 patients with amblyopia and finding that they all had their amblyopic (low visual activity) eye closed in early life, following an eye operation, with most of the closures occurring within the first year of life (Awaya et al., 1973). This type of amblyopia is called stimulus-deprivation amblyopia.
Figure 6:4: Ocular dominance histogram of a kitten that had one eye occluded for 24 hours following four weeks of normal vision (redrawn from Olson & Freeman, 1975).
Figure 6:5: Profile of the sensitive period for monocular deprivation in kittens. As can be seen, the most sensitive period is at 4 to 6 weeks, but monocular deprivation can cause substantial effects as long as 4 months after birth (redrawn from Olson & Freeman, 1975).
Image misalignment and binocularity
The changes in the ocular dominance columns are merely the most obvious effect of changes in the balance of neural input into the visual cortex. The majority of cells in the normal visual cortex are binocular, and during post-natal development, when the ocular dominance columns are being established, the connections to individual
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cells from both eyes are also being refined. Unsurprisingly, monocular deprivation leads to most cells in the visual cortex being monocular. Under normal conditions, the input to a cell from the two red eyes is from corresponding areas of the retina. Misalignment of the images in the two eyes can be accomplished either by cutting the eye muscles or by fitting the animal with a helmet that contains small optical prisms. This disruption does not alter the absolute magnitude of activity. Under these conditions, most cells can only be driven monocularly, rather than binocularly as in normal animals, and the ocular dominance columns seem more sharply delineated (Lowel & Singer, 1993). Whereas 80% of cortical cells in normal cats are binocular, only 20% of the cells in cats with cut eye muscles respond to the stimulation of both eyes (Hubel & Wiesel, 1965). Similarly, 70% of cortical cells in monkeys are binocular, but less than 10% of cells are binocular in a monkey that has worn a prism-helmet for 60 days (Crawford & von Noorden, 1980). These neurological changes translate into striking behavioural effects. For example, prism-reared monkeys are unable to detect depth in random-dot stereograms, suggesting that they have lost the ability to use binocular disparity to perceive depth (Crawford et al., 1984).
It appears that it is not just the magnitude or balance of neural activity that is important, but also the temporal pattern of this activity. This hypothesis is supported by experiments in which the retina was deactivated with tetrodotoxin, and the optic nerve was stimulated directly. This allowed the temporal relationship of the neural activity from the two eyes to be controlled directly. Many more cortical cells were found to be monocular under a regimen of separate stimulation through the two optic nerves than were found with simultaneous stimulation (Stryker & Strickland, 1984). This synchronised activity of the two inputs to the same cell could be used in a Hebbian process for strengthening synapses from both inputs. The mechanism of this strengthening could be a form of LTP called ‘associative LTP’, in which the paired activity of two inputs to a cell results in the strengthening of both inputs. Uncorrelated activity from the two eyes seems to lead to a weakening and possible elimination of synapses in the visual cortex. This is another form of neural plasticity, long-term depression (LTD). A similar result can be demonstrated in the development of orientation selectivity by V1 neurons. If electrical stimulation is used to introduce artificially correlated activity into the visual system, the development of orientation selectivity is disrupted, emphasising once again how important the relative temporal pattern of activity is for developing neural connectivity (Weliky & Katz, 1997; Weliky, 2000).
Image misalignment in humans
Some people have an imbalance in the eye muscles that upsets the co-ordination between their two eyes. This condition is called strabismus.
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Figure 6:6: Stimuli for measuring the tilt aftereffect. If you stare at the adaptation pattern on the left for 60 s and then turn your gaze on to the test pattern to the right, you see the test lines as tilted. This is the tilt after-effect.
The misaligned eye can either turn inwards (esotropia) or outwards (exotropia). Just as cutting the eye muscles in experimental animals causes a loss of cortical cells that respond to stimulation of both eyes, there seems to be a similar lack of binocularly driven cells in people who had strabismus as young children. Strabismus can be corrected by a muscle operation that restores the balance between the two eyes. However, if this operation is not performed until the child is 4–5 years of age, a loss of binocularly driven cells seems to occur. This can be measured by the tilt after effect (Figure 6.6), because of the phenomenon of interocular transfer. If an observer looks at the adapting lines with one eye and then looks at the test lines with the other eye, the after-effect will transfer between the eyes. This transfer, which is about 60%–70% as strong as the effect that occurs if the adaptation and test lines are viewed with the same eye, indicates that information from one eye must be shared with the other. The degree of transfer can be used to assess the state of binocularly driven cells. When surgery is carried out early in life, interocular transfer is high, indicating good binocular function, but if the surgery is delayed, interocular transfer is poor, indicating poor binocular function. The critical period for binocular development in humans seems to begin during the first year of life, reaches a peak during the second year, and decreases by 4 to 8 years (Banks, Aslin & Letson, 1975) (Figure 6.7).
The reduction in binocular neurons in people with strabismus reduces their ability to see depth, as much of our depth perception comes from comparing the differences in visual input between the eyes (see Chapter 11). However, in some cases this reduced depth perception might actually be an advantage. An artist has to translate the complexity of the 3-D world into a 2-D picture. It might be an advantage if you already see the world as a flat, 2-D image. A possible artistic candidate for this phenomenon is the seventeenth-century Dutch painter, Rembrandt van Rijn (Figure 6.8). An analysis of a set of his self-portraits (24 oil paintings and 12 etchings) showed that, in all but one painting, the eye on the right of the painting looked straight ahead, and the one on the left looked outwards (Livingstone & Conway, 2004). This eye alignment suggests exotropic strabismus.
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Figure 6:7: The degree of interocular transfer of the tilt aftereffect as a function of the age at which surgery was performed to correct strabismus (after Banks, Aslin & Letson, 1975).
Figure 6:8: Self-portrait Leaning on a Stone Wall (detail). The etching by Rembrandt in 1639 (reprinted with the permission of the British Museum).
As the authors of this study point out, art students are often advised to close one eye to flatten their perception, and so, for an artist, this impaired depth perception might be an advantage, rather than a handicap.
Selective rearing: manipulating the environment
Another way of altering the visual input is to raise animals in a tightly controlled visual environment, dominated by a certain visual stimulus and deficient in others. This does not alter the balance of activity between the eyes, but does alter the pattern of activity produced by each eye. These experiments have usually been carried out either by placing infant animals in an environment containing stripes of only one orientation (e.g. Blakemore & Cooper, 1970) or by fixing infant animals with goggles that present vertical stripes to one eye and horizontal stripes to the other (e.g. Hirsch & Spinelli, 1970).
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Blakemore and Cooper kept kittens in the dark from birth to 2 weeks of age and then placed them in a large vertical tube for 5 hours every day. For the rest of the day, they remained in the dark. The inner surface of the tube was covered with either horizontal or vertical stripes. The kittens sat on a plexi-glass floor and the tube extended above and below them to ensure that there were no visible corners or edges in their environment other than the stripes on the side of the tube. The kittens wore neck ruffs to prevent them altering the orientation of the stripes by turning their heads. After 5 months, the selective rearing was stopped and the kittens remained in the dark except for brief periods when their vision was tested. The kittens displayed a number of defects in their visual behaviour. Their head movements were jerky when following moving objects, they tried to touch distant objects and often bumped into things. Most important of all, they seemed to be blind to stripes orthogonal to the orientation of the environment in which they were reared. Following these behavioural tests, Blakemore and Cooper recorded from cells in the visual cortex to determine the optimum stimulus orientation for different cells. Most of the cells of the ‘horizontally reared’ cats responded primarily to horizontal stimuli and none at all responded to vertical stimuli. The opposite is true of the ‘vertically reared’ cats. These results have been confirmed by subsequent experiments (Muir & Mitchell, 1975). The results of Hirsch and Spinelli’s experiments (1970) using goggles showed the same pattern of effects. In single-cell recording experiments, they have found few cells in the visual cortex where the preferred orientation deviated from the orientation of the environmental stimulus by more than 5–10 degrees.
A single hour of exposure in a striped tube can drastically alter the preferred orientation of cells in the visual cortex. Blakemore and Mitchell (1973) kept a kitten in the dark until they recorded from its visual cortex at 42 days of age. As in kittens exposed to vertical stripes for much longer periods of time, most cells responded best to vertical or near-vertical orientations.
A number of different types of environment have been used to explore cortical plasticity further, such as moving white spots, random arrays of point sources of light and stripes moving in one particular direction (e.g. Van Sluyters & Blakemore, 1973; Pettigrew & Freeman, 1973). In each case the majority of cortical cells responded to the stimuli that were present in their environment and responded very weakly to anything else. An interesting example of selective rearing is shown in cats reared under conditions of stroboscopic illumination, where continuous retinal movement is prevented. This results in a deficit in the direction selectivity of the cortical cells, which is expressed behaviourally as a deficit in motion perception (Cynader & Cherneneko, 1976). The development of other cortical cell properties, such as orientation and stereo-selectivity, is unaffected.
It seems that, during the critical period, a number of changes are made to the wiring of the visual system, and this fine tuning is activity dependent. Without neural activity to stimulate and alter