Linear mechanisms of directional selectivity in simple cells of cat striate cortex.

Abstract

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...

Adaptive Temporal Integration of Motion in Direction-Selective Neurons in Macaque Visual Cortex

“…Could these stimulus-related changes at the perceptual level originate from changes in the properties of single cortical DS cells, or do they simply reflect a population of diverse, but individually fixed, temporal RF profiles? Fixed RFs are consistent with demonstrations that linear spatiotemporal filters account well for response properties including direction selectivity in V1 simple cells (Movshon et al, 1978;Reid et al, 1987;Palmer, 1989, 1994;DeAngelis et al, 1993), but there have been some reports of stimulus-related changes in temporal integration in simple and complex cells in cats and monkeys (Dean et al, 1982;Reid et al, 1992).…”

Temporal Properties of Inputs to Direction-Selective Neurons in Monkey V1

“…Inseparable simple cell receptive fields have been described in detail (Albrecht and Geisler 1991;Dean and Tolhurst 1986;DeAngelis et al 1993;Jagadeesh et al 1997;McLean and Palmer 1989;McLean et al 1994;Movshon et al 1978;Murthy et al 1998;Reid et al 1987;Saul and Humphrey 1992b). Several clear results have emerged.…”

The accuracy of membrane potential reconstruction based on spiking receptive fields

“…Simple cell spiking responses deviate significantly from linear expectations, but the underlying basis for the differences between predicted and actual values is unclear. Spiking responses based on noise stimulation systematically underestimate spiking selectivity for orientation tuning (Gardner et al 1999), spatial and temporal frequency (DeAngelis et al 1993b), direction (Albrecht and Geisler 1991;DeAngelis et al 1993b;Reid et al 1987Reid et al , 1991, and binocular disparity . As in previous reports, we found that our expectation of response (GP SP ), derived from the spiking responses to the noise stimulus, is related to recorded spike rate in a nonlinear fashion (Fig.…”