Evidence for long-term functional plasticity in the visual cortex of adult cats

Abstract

1. Vision was investigated with behavioural and electrophysiological techniques in three groups of cats: (a) two normally raised kittens in which one eye was rotated at an age of 3 months, (b) three adult cats in which one eye had been rotated and the other closed 6 months prior to recording, (c) two adult cats in which first one eye had been rotated and the other closed and subsequently, after one year, the rotated eye had been closed and the normal eye re-opened. The latter two cats were investigated 6 and 12 months after reverse suture, respectively. All adult cats were at least 2 years old when operated on for the first time.2. Behavioural analysis revealed that the kittens of the first group no longer used the rotated eye for fixation, visuo-motor behaviour being impaired when tested through this eye. Binocularity was found to be disrupted to nearly the same extent as in kittens made strabismic at the beginning of the critical period. In addition, ocular dominance was shifted towards the normal eye.3. The adult cats in the second group developed a virtually complete neglect of the visual modality subsequent to a period of severely disturbed visuo-motor behaviour.4. These behavioural abnormalities were associated with clear alterations in the functional state of striate cortex. Only 47% of the recorded cells could be driven with light, the majority of these reactive neurones yielding only sluggish responses to optimally aligned stimuli. The ocular dominance distribution showed a significant reduction of binocular cells but gave no indication of a shift in ocular dominance towards either of the two eyes. Moreover, contrast sensitivity as assessed with pattern-evoked potentials was significantly reduced.5. The remaining two animals that were reverse sutured after the visual neglect had developed showed complete behavioural recovery when tested through the re-opened normal eye. However, this recovery was not instantaneous and occurred only after the cats had been forced to use their visual sense.6. Behavioural recovery was paralleled by an increase of cortical reactivity to normal levels and by a marked increase in binocularity. This gain increase of excitatory transmission was, however, selective for neurones dominated by the normal eye, leading to a bias in ocular dominance towards this eye.7. The observed modifications in the functional state of striate cortex indicate that reversible changes in the gain of excitatory transmission can still occur beyond the end of the classical critical period. These long-lasting changes in synaptic efficiency appear to follow the rules postulated by Hebb for adaptive synaptic connexions.