Synaptic plasticity in visual cortex: Comparison of theory with experiment

1. The aim of this work was to assess whether a form of synaptic modification based on the theory of Bienenstock, Cooper, and Munro (BCM) can, with a fixed set of parameters, reproduce both the kinetics and equilibrium states of experience-dependent modifications that have been observed experimentally in kitten striate cortex. 2. According to the BCM theory, the connection strength of excitatory geniculocortical synapses varies as the product of a measure of input activity (d) and a function (φ) of the summed postsynaptic response. For all postsynaptic responses greater than spontaneous but less than a critical value called the 'modification threshold' (θ), φ has a negative value. For all postsynaptic responses greater than θ, φ has a positive value. A novel feature of the BCM theory is that the value of θ is not fixed, but rather 'slides' as a nonlinear function of the average postsynaptic response. 3. This theory permits precise specification of theoretical equivalents of experimental situations, allowing detailed, quantitative comparisons of theory with experiment. Such comparisons were carried out here in a series of computer simulations. 4. Simulations are performed by presenting input to a model cortical neuron, calculating the summed postsynaptic response, and then changing the synaptic weights according to the BCM theory. This process is repeated until the synaptic weights reach an equilibrium state. 5. Two types of geniculocortical input are simulated: 'pattern' and 'noise.' Pattern input is assumed to correspond to the type of input that arises when a visual contour of a particular orientation is presented to the retina. This type of input is said to be 'correlated' when the two sets of geniculocortical fibers relaying information from the two eyes convey the same patterns at the same time. Noise input is assumed to correspond to the type of input that arises in the absence of visual contours and, by definition, is uncorrelated. 6. By varying the types of input available to the two sets of geniculocortical synapses, we simulate the following types of visual experience: 1) normal binocular contour vision, 2) monocular deprivation, 3) reverse suture, 4) strabismus, 5) binocular deprivation, and 6) normal contour vision after a period of monocular deprivation. 7. The constraints placed on the set of parameters by each type of simulated visual environment, and the effects that such constraints have on the evolution of the synaptic weights, are investigated in detail. 8. It was discovered that the exact form and dependencies of the sliding modification threshold are critical in obtaining a set of simulations that are consistent with the experimentally observed kinetics of synaptic modification in visual cortex. In particular, to account for observed changes during reverse suture and binocular deprivation, the value of θ could approach zero only when the synaptic strengths were driven to very low values. In the present model, this was achieved by including in the calculation of θ the postsynaptic responses generated by spontaneous input activity. 9. It is concluded that the modification of excitatory geniculocortical synapses according to rules derived from the BCM theory can account for both the outcome and kinetics of experience-dependent synaptic plasticity in kitten striate cortex. The understanding that this theory provides should be useful for the design of neurophysiological experiments aimed at elucidating the molecular mechanisms in play during the modification of visual cortex by experience.