Theory for the Development of Neuron Selectivity : Orientation Specificity and Binocular Interaction in Visual Cortex

Abstract

The development of stimulus selectivity in the primary sensory cortex of higher vertebrates is considered in a general mathematical framework. A synaptic evolution scheme of a new kind is proposed in which incoming patterns rather than converging afferents compete. The change in the efficacy of a given synapse depends not only on instantaneous pre-and postsynaptic activities but also on a slowly varying time-averaged value of the postsynaptic activity. Assuming an appropriate nonlinear form for this dependence, development of selectivity is obtained under quite general conditions on the sensory environment. One does not require nonlinearity of the neuron's integrative power nor does one need to assume any particular form for intracortical circuitry. This is first illustrated in simple cases, e.g., when the environment consists of only two different stimuli presented alternately in a random manner. The following formal statement then holds: the state of the system converges with probability 1 to points of maximum selectivity in the state space. We next consider the problem of early development of orientation selectivity and binocular interaction in primary visual cortex. Giving the environment an appropriate form, we obtain orientation tuning curves and ocular dominance comparable to what is observed in normally reared adult cats or monkeys. Simulations with binocular input and various types of normal or altered environments show good agreement with the relevant experimental data. Experiments are suggested that could test our theory further.It has been known for some time that sensory neurons at practically all levels display various forms of stimulus selectivity. They may respond preferentially to a tone of a given frequency, a light spot of a given color, a light bar of a certain length, retinal disparity, orientation, etc. We might, therefore, regard stimulus selectivity as a general property of sensory neurons and conjecture that the development of such selectivity obeys some general rule. Most attractive is the idea that some of the mechanisms by which selectivity develops in embryonic or early postnatal life are sufficiently general to allow a unifying theoretical treatment.