Hebbian models of development and learning require both activity-dependent synaptic plasticity and a mechanism that induces competition between different synapses. One form of experimentally observed long-term synaptic plasticity, which we call spike-timing-dependent plasticity (STDP), depends on the relative timing of pre- and postsynaptic action potentials. In modeling studies, we find that this form of synaptic modification can automatically balance synaptic strengths to make postsynaptic firing irregular but more sensitive to presynaptic spike timing. It has been argued that neurons in vivo operate in such a balanced regime. Synapses modifiable by STDP compete for control of the timing of postsynaptic action potentials. Inputs that fire the postsynaptic neuron with short latency or that act in correlated groups are able to compete most successfully and develop strong synapses, while synapses of longer-latency or less-effective inputs are weakened.

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The origin of orientation selectivity in visual cortical responses is a central problem for understanding cerebral cortical circuitry. In cats, many experiments suggest that orientation selectivity arises from the arrangement of lateral geniculate nucleus (LGN) afferents to layer 4 simple cells. However, this explanation is not sufficient to account for the contrast invariance of orientation tuning. To understand contrast invariance, we first characterize the input to cat simple cells generated by the oriented arrangement of LGN afferents. We demonstrate that it has two components: a spatial-phase-specific component (i.e., one that depends on receptive field spatial phase), which is tuned for orientation, and a phase-nonspecific component, which is untuned. Both components grow with contrast. Second, we show that a correlation-based intracortical circuit, in which connectivity between cell pairs is determined by the correlation of their LGN inputs, is sufficient to achieve well tuned, contrast-invariant orientation tuning. This circuit generates both spatially opponent, "antiphase" inhibition ("push-pull"), and spatially matched, "same-phase" excitation. The inhibition, if sufficiently strong, suppresses the untuned input component and sharpens responses to the tuned component at all contrasts. The excitation amplifies tuned responses. This circuit agrees with experimental evidence showing spatial opponency between, and similar orientation tuning of, the excitatory and inhibitory inputs received by a simple cell. Orientation tuning is primarily input driven, accounting for the observed invariance of tuning width after removal of intracortical synaptic input, as well as for the dependence of orientation tuning on stimulus spatial frequency. The model differs from previous push-pull models in requiring dominant rather than balanced inhibition and in predicting that a population of layer 4 inhibitory neurons should respond in a contrast-dependent manner to stimuli of all orientations, although their tuning width may be similar to that of excitatory neurons. The model demonstrates that fundamental response properties of cortical layer 4 can be explained by circuitry expected to develop under correlation-based rules of synaptic plasticity, and shows how such circuitry allows the cortex to distinguish stimulus intensity from stimulus form.