Initial recovery of vision after early monocular deprivation in kittens is faster when both eyes are open

Abstract

A comparison was made of the speed of visual recovery in the deprived eye of kittens after a 6-day period of monocular deprivation imposed at 5-9 weeks of age in two postdeprivation conditions. In one condition, binocular recovery (BR), both eyes were open, whereas in the other condition, reverse lid-suture (RLS), the formerly nondeprived eye was closed to force the animal to use the originally deprived eye. In littermate pairs, BR kittens began to recover form vision 12 to 30 h before those subjected to RLS. The vision of the deprived eye of the BR animals remained superior to that of their RLS littermates for 4-8 days. Although this finding is difficult to reconcile with competitive mechanisms of synaptic plasticity, it supports a prediction of an alternative model of synaptic plasticity [Bienenstock, E. L., Cooper, L. N. & Munro, P. W. (1982) J. Neurosci. 2, 32-48] for slower initial recovery with RLS because of the time required to reset the modification threshold.

Figure 1

(A) A sketch (not to scale) of the jumping stand used to measure visual acuity. Kittens were trained to jump from a platform (P) to a vertical grating that was separated by a divider from an adjacent horizontal grating of the same period. See text for details. (B) The MAR of the deprived eye of C844B (○) and C842R (●) as a function of recovery time. The lines through the data represent the best-fitting power functions to the MAR values excluding all data obtained following attainment of the lowest MAR value after approximately 10 days.

Figure 2

The MAR of the deprived eye as a function of recovery time for three other littermate comparisons of BR (○) and RLS (●).

Figure 3

(A) The BCM model. The synaptic weight of a particular synapse changes in time as a linear function of the presynaptic activity and a nonlinear function (φ), of the postsynaptic activity (c) and the modification threshold (θ_m) that is a function of the time-averaged postsynaptic activity of the cell. According to the BCM model, synaptic strengthening of a synapse occurs when presynaptic activity is sufficient to cause depolarization of the postsynaptic cell above the modification threshold, whereas levels of depolarization below this threshold leads to synaptic weakening. See Methods for further details. (B) The predicted changes with time in the synaptic weights (M_L) with the deprived (left) eye for the two recovery conditions. C_L and C_R represent the level of postsynaptic activity attributable to stimulation of, respectively, either the left (deprived) or right eye. In the situation of BR, C_L+R represents the postsynaptic activity resulting from simultaneous stimulation of both eyes. For the RLS condition, the original modification threshold at time t₀ is designated as θ_m0, whereas θ_m1 and θ_m2 refer to its level at t₁ and t₂, respectively. The φ function for the RLS condition is indicated at three points in time by the filled line; the dashed line depicts this function at time t₀. Data from our experiments suggest that resetting of the modification threshold requires 12–30 h depending on the state of developmental plasticity (i.e., the age of the kitten when monocularly deprived).