Strabismus does not prevent recovery from monocular deprivation: A challenge for simple Hebbian models of synaptic modification

Abstract

It has been suggested that development of central connections in the mammalian visual system is governed by a simple Hebbian rule of synaptic modifiability. Under such a rule, simultaneity of presynaptic and postsynaptic action potentials is a prerequisite for enhanced synaptic efficacy. The present paper reports the results of a study designed to test whether this hypothesis is applicable to the development of the thalamo-cortical visual pathway. In four-week-old kittens, exposure to a 2-d period of monocular deprivation was used to render the vast majority of cortical cells capable of being activated only by the nondeprived eye. During a subsequent 3-5 month recovery period, both eyes were open but surgically misaligned. This combination of conditions was chosen so that during the recovery period presynaptic activity originating from the initially deprived eye would be decorrelated from postsynaptic action potentials in cortical neurons. If synaptic modification is regulated by a simple Hebbian mechanism, then in this situation the deprived eye should be unable to recover control of cortical cells. In fact, the present results indicate that during the recovery period the proportion of cortical neurons dominated by the deprived eye rose to a level equal to that of the nondeprived eye--a result contrary to that predicted by a simple Hebbian rule of development. Histological analysis indicated that a similar level of recovery was present both within and outside of cortical layer IV, the main thalamo-recipient layer. As expected, the induced strabismus resulted in a failure of cortical binocularity to recover in these kittens. Although these results argue against a simple Hebbian mechanism of development, they are compatible with the hypothesis that synaptic modifiability is dependent upon correlations between presynaptic activity and local, subthreshold, postsynaptic changes. This alternative hypothesis has the advantage of allowing modification of local synaptic circuits within the dendritic arbors of a single neuron.