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We recorded the responses of direction-selective simple and complex cells in the primary visual cortex (V1) of anesthetized, paralyzed macaque monkeys. When studied with sine-wave gratings, almost all simple cells in V1 had responses that were separable for spatial and temporal frequency: the preferred temporal frequency did not change and preferred speed decreased as a function of the spatial frequency of the grating. As in previous recordings from the middle temporal visual area (MT), approximately one-quarter of V1 complex cells had separable responses to spatial and temporal frequency, and one-quarter were “speed tuned” in the sense that preferred speed did not change as a function of spatial frequency. Half fell between these two extremes. Reducing the contrast of the gratings caused the population of V1 complex cells to become more separable in their tuning for spatial and temporal frequency. Contrast dependence is explained by the contrast gain of the neurons, which was relatively higher for gratings that were either both of high or both of low temporal and spatial frequency. For stimuli that comprised two spatially superimposed sine-wave gratings, the preferred speeds and tuning bandwidths of V1 neurons could be predicted from the sum of the responses to the component gratings presented alone, unlike neurons in MT that showed nonlinear interactions. We conclude that spatiotemporal modulation of contrast gain creates speed tuning from separable inputs in V1 complex cells. Speed tuning in MT could be primarily inherited from V1, but processing that occurs after V1 and possibly within MT computes selective combinations of speed-tuned signals of special relevance for downstream perceptual and motor mechanisms.

Tuning for speed is one key feature of motion-selective neurons in the middle temporal visual area of the macaque cortex (MT, or V5). The present paper asks whether speed is coded in a way that is invariant to the shape of the moving stimulus, and if so, how. When tested with single sine-wave gratings of different spatial and temporal frequencies, MT neurons show a continuum in the degree to which preferred speed depends on spatial frequency. There is some dependence in 75% of MT neurons, and the other 25% maintain speed tuning despite changes in spatial frequency. When tested with stimuli constructed by adding two superimposed sine-wave gratings, the preferred speed of MT neurons becomes less dependent on spatial frequency. Analysis of these responses reveals a speed-tuning nonlinearity that selectively enhances the responses of the neuron when multiple spatial frequencies are present and moving at the same speed. Consistent with the presence of the nonlinearity, MT neurons show speed tuning that is close to form-invariant when the moving stimuli comprise square-wave gratings, which contain multiple spatial frequencies moving at the same speed. We conclude that the neural circuitry in and before MT makes no explicit attempt to render MT neurons speed-tuned for sine-wave gratings, which do not occur in natural scenes. Instead, MT neurons derive form-invariant speed tuning in a way that takes advantage of the multiple spatial frequencies that comprise moving objects in natural scenes.

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.