CONTRAST-INVARIANT ORIENTATION TUNING IN CAT VISUAL-CORTEX - THALAMOCORTICAL INPUT TUNING AND CORRELATION-BASED INTRACORTICAL CONNECTIVITY

The origin of orientation selectivity in visual cortical responses is a central problem for understanding cerebral cortical circuitry. In ca ts, 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 accoun t for the contrast invariance of orientation tuning. To understand con trast 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 fo r orientation, and a phase-nonspecific component, which is untuned. Bo th components grow with contrast. Second, we show that a correlation-b ased intracortical circuit, in which connectivity between cell pairs i s determined by the correlation of their LGN inputs, is sufficient to achieve well tuned, contrast-invariant orientation tuning. This circui t generates both spatially opponent, ''antiphase'' inhibition (''push- pull''), and spatially matched, ''same-phase'' excitation. The inhibit ion, if sufficiently strong, suppresses the untuned input component an d sharpens responses to the tuned component at all contrasts. The exci tation amplifies tuned responses. This circuit agrees with experimenta l evidence showing spatial opponency between, and similar orientation tuning of, the excitatory and inhibitory inputs received by a simple c ell. Orientation tuning is primarily input driven, accounting for the observed invariance of tuning width after removal of intracortical syn aptic input, as well as for the dependence of orientation tuning on st imulus spatial frequency. The model differs from previous push-pull mo dels in requiring dominant rather than balanced inhibition and in pred icting that a population of layer 4 inhibitory neurons should respond in a contrast-dependent manner to stimuli of all orientations, althoug h their tuning width may be similar to that of excitatory neurons. The model demonstrates that fundamental response properties of cortical l ayer 4 can be explained by circuitry expected to develop under correla tion-based rules of synaptic plasticity, and shows how such circuitry allows the cortex to distinguish stimulus intensity from stimulus form .