The Critical Period for Experience-dependent Plasticity in a System of Binocular Visual Connections in Xenopus...

A commissural system of 'intertectal' connections in Xenopus mediates the registration of binocular visual maps at the midbrain optic tectum. Following surgical eye rotation in larval animals, the system can completely alter its pattern of connectivity to restore binocular visual registration at the tectum. This experimentally induced plasticity is known to require visual experience and thought to be subject to an age-related restriction: eye rotation in adult animals is reported to provoke no subsequent intertectal alteration. In this paper we describe the detailed age-dependence of this plasticity. One eye was rotated in 238 animals of various developmental stages between mid-larval and adult life. At each age, different animals received rotations of different sizes, ranging from 20 to 180 degrees. The pattern of intertectal connectivity was mapped electrophysiologically 1 - 2 years postoperatively. A 'critical' period was defined around the time of metamorphosis: the vast majority of animals receiving a rotation in larval life (up to approximately 2 weeks before metamorphic climax) showed altered intertectal connections, whereas none of the animals operated upon at 3 months or more postmetamorphosis displayed the plasticity. At intervening ages, altered intertectal connections were found only in response to progressively smaller eye rotations. The profile of this critical period was further shown to mirror temporal features of the changes in eye position that occur in Xenopus as natural consequences of head growth, and which themselves impose a normal developmental requirement for intertectal plasticity. We conclude that the capacity of the Xenopus intertectal system for plasticity in response to abnormal experience undergoes a progressive age-dependent decline, and that the profile of this decline is delimited by normal requirements.