1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)

The role of linear spatial summation in the directional selectivity of simple cells in cat striate cortex was investigated. The experimental paradigm consisted of comparing the response to drifting grating stimuli with linear predictions based on the response to stationary contrast-reversing gratings. The spatial phase dependence of the response to contrast-reversing gratings was consistent with a high degree of linearity of spatial summation within the receptive fields. Furthermore, the preferred direction predicted from the response to stationary gratings generally agreed with the measurements made with drifting gratings. The amount of directional selectivity predicted was, on average, about half the measured value, indicating that nonlinear mechanisms act in concert with linear mechanisms in determining the overall directional selectivity.Directional selectivity of receptive fields is pervasive in the mammalian visual system, occurring as early as the retinal ganglion cell level (1, 2). However, the directionally selective ganglion cells project to brainstem centers (3, 4) and are not responsible for the directional selectivity of cat striate cortex neurons. In the geniculostriate system of the cat, directional selectivity first appears in simple cells of primary visual cortex (5), from nondirectional X and Y cell input (6-8). Previously (9), it was shown that a simple cell receptive field model composed of a linear summation of lateral geniculate nucleus (LGN) inputs could qualitatively account for both the orientation tuning and directional selectivity of these cortical neurons. The basis of the directional selectivity was a differential alteration of the temporal response characteristics of the LGN inputs, presumably mediated by intracortical circuitry. In this report, we provide experimental evidence demonstrating that directional selectivity of simple cells in area 17 of the cat does in fact result from linear spatial summation within the receptive field. Portions of this work have appeared in abstract form (10,11).Though previous investigations of simple cell directional selectivity have been mainly concerned with the role of nonlinear interactions (12), the involvement of linear spatial summation can be addressed in a rigorous, straightforward manner. A linear receptive field composed of an asymmetric arrangement of an and off regions will not be directionally selective if the temporal properties of the on and off regions are the same. Although drifting gratings will reveal the absence of directional selectivity in this type of receptive field, it will appear to be directionally selective if tested only with light bars. However, its "preferred direction" will reverse with a change in stimulus contrast signature-i.e., when tested with dark bars (1). This is not the case for most simple cells, which have the same preferred direction for light and dark bars (13,14). For a neuron with linear spatial summation to show directional selectivity, two requirements must be met. The first of these requirem...

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1. The orientation tuning of lateral geniculate nucleus (LGN) neurons and retinal ganglion cells (recorded as S potentials in the LGN) was investigated with drifting grating stimuli. 2. Results were compared with a quantitative model, in which receptive fields were constructed from linear, elliptical Gaussian center and surround subunits, and responses could be predicted to gratings of any spatial frequency at any orientation. 3. The orientation tuning of X and Y retinal ganglion cells and LGN neurons was shown to result from the linear mechanism of receptive-field elongation, as data from these cells could be well fit with this model. 4. The responses of LGN neurons and their input retinal ganglion cells were compared. The orientation tuning of LGN neurons was found to be a reflection of the tuning of their retinal inputs, showing that neither intrageniculate neural interactions nor the corticogeniculate projection play any role in LGN orientation selectivity.

1. The response properties of accessory optic system (AOS) neurons were assessed using single-unit extracellular recording from each of the three AOS terminal nuclei [medial, lateral, and dorsal terminal nuclei (MTN, LTN, and DTN)] in the anesthetized rabbit. 2. AOS neurons had large, monocular (contralateral) receptive fields (tens of degrees on a side) and exhibited a pronounced selectivity to the speed and direction of movement of large, textured patterns. The greatest responses occurred at slow speeds on the order of 0.5 degrees/s. 3. MTN and LTN neurons responded best to movement in near vertical directions. However, the stimulus directions corresponding to the greatest excitation and the greatest inhibition both had a posterior component and, thus, the preferred excitatory and inhibitory directions were not opposite each other. DTN neurons responded most strongly to horizontal movement and were excited by temporal to nasal movement. 4. AOS neurons were unresponsive to natural vestibular stimulation presented as sinusoidal oscillations of the rabbit about the yaw, pitch, and roll axes. 5. The response properties of AOS neurons are remarkably similar to those of the ON, direction-selective ganglion cells of the rabbit retina, and therefore this class of ganglion cell is most likely the predominant, if not the only, direct retinal input to the AOS. The local direction-selective properties of AOS neurons can be accounted for by combining the tuning curves of ON, direction-selective ganglion cells in a simple manner. 6. The low speed preference of AOS neurons, along with their large receptive fields suggests that they are suited to complement the vestibular system in detecting self-motion.