Time course of suppression by surround gratings: Highly contrast-dependent, but consistently fast

Abstract

Timing is critical for the effectiveness of a modulating surround signal. In this study, the optimal timing of a suppressing surround signal was measured psychophysically in human subjects. The perceived contrast of a fixated 1-deg circular patch of vertical sinusoidal grating (the target: 4 cpd, Michelson contrast 0.2) was measured as a function of the onset asynchrony between the target and an annular "surround" grating with the same orientation and spatial frequency. The contrast and area of the surround stimulus were varied parametrically. The suppressive signal peaked at earlier times the higher the surround contrast (0.1-0.4), following a function consistent with the contrast-dependence of retinal response dynamics. Increasing the area of the surround grating also moved peak suppression to earlier times. At ca. 2 deg annulus outer diameter the time to peak of the suppressive signal was shortest, although its amplitude grew with annulus area even beyond that. When both the contrast and the area of the centre and surround gratings were equal, suppression was maximal if the surround stimulus was presented ca. 5 ms before the target. Such a short delay of suppression is consistent with a neural implementation based on feedforward-feedback connections, but not with horizontal connections.

Effects of Mean Luminance Changes on Human Contrast Perception: Contrast Dependence, Time-Course and Spatial Specificity

“…In addition, the reliability of the neural or perceptual representations of stimuli are likely to be affected as the early part of neural responses, which is generally considered the most reliable part [38], [39], [40], is especially vulnerable to the effect of a simultaneous change of luminance and contrast. Finally, to offer some perspective, the magnitude and duration of the observed effects are comparable to those found for cross-orientation overlay masking [41] and iso-orientation surround suppression [42]. These effects are generally considered to be perceptually relevant.…”

Multiple components of surround modulation in primary visual cortex: Multiple neural circuits with multiple functions?

“…It is our opinion that these authors' argument is only partly valid, since surround suppression does occur at the fovea when the contrast of the target is above threshold, i.e. when suppression is measured either using supra-threshold contrast matching (Cannon & Fullenkamp, 1991, 1993; Chubb, Sperling, & Solomon, 1989; Ejima & Takahashi, 1985; Kilpeläinen, Donner, & Laurinen, 2007; Nurminen, Peromaa, & Laurinen, 2010; Olzak & Laurinen, 1999; Snowden & Hammett, 1998; Solomon, Sperling, & Chubb, 1993; Xing & Heeger, 2000, 2001) or detection on a pedestal (Chen & Tyler, 2002; Snowden & Hammett, 1998; Yu & Levi, 1997) tasks. Moreover, the argument that the spatial extent of surround modulation does not scale with spatial frequency is controversial, because the spatial extent of near-surround modulation does scale at supra-threshold contrast, at least up to 4.8 cycles surround width (Cannon & Fullenkamp, 1991).…”

“…These distances exceed the visuotopic reach of monosynaptic horizontal connections in V1 (Angelucci et al, 2002). While polysynaptic chains of horizontal connections could in principle underlie the far-surround effects, the conduction velocity of horizontal axons is too slow (Girard, Hupé, & Bullier, 2001) to account for the very fast onset of orientation-tuned surround suppression in V1 cells (Bair, Cavanaugh, & Movshon, 2003) and human vision (Kilpeläinen, Donner, & Laurinen, 2007). Moreover, if horizontal connections mediated far-surround modulation, the latency of suppression should be strongly distance dependent, but experiments show that it is nearly independent of the distance of the surround stimulus from the RF (Bair, Cavanaugh, & Movshon, 2003).…”

“…Feedback projections from areas V2, V3 and MT convey information to V1 from a visual field region corresponding on average to 5, 10 and 25 times, respectively, the RF size of V1 neurons. Moreover, feedback axons have high conduction velocities (Girard, Hupé, & Bullier, 2001), and therefore are well suited to mediate the very fast far-surround modulation (Bair, Cavanaugh, & Movshon, 2003; Kilpeläinen, Donner, & Laurinen, 2007). …”

Circuits and Mechanisms for Surround Modulation in Visual Cortex

“…In primates, the monosynaptic extent of horizontal connections is insufficient to account for the spatial extent of the far-surround (Angelucci et al 2002). Polysynaptic chains of horizontal axons are unlikely to generate far-SM because their conduction velocity, at least in the superficial layers (0.1–0.3 m/s), is too slow (Grinvald et al 1994, Bringuier et al 1999, Girard et al 2001, Slovin et al 2002, Benucci et al 2007) to account for the fast onset of far-SM in V1 cells (10–30 ms; see Section 2.1; for a detailed discussion, see Angelucci & Shushruth 2013) and in human perception (Kilpelainen et al 2007). It remains to be determined whether horizontal axons in infragranular layers have faster conduction velocities (1m/s; (Girard et al 2001) that could account for far-SM in these layers.…”