Different Orientation Tuning of Near- and Far-Surround Suppression in Macaque Primary Visual Cortex Mirrors Their Tuning in Human Perception

Abstract

In primary visual cortex (V1) neuronal responses to stimuli inside the receptive field (RF) are usually suppressed by stimuli in the RF surround. This suppression is orientation-specific. Similarly, in human vision surround stimuli can suppress perceived contrast of a central stimulus in an orientation-dependent manner. The surround consists of two regions likely generated by different circuits: a near-surround generated predominantly by geniculocortical and intra-V1 horizontal connections, and a far-surround generated exclusively by inter-areal feedback. Using stimuli confined to the near- or far-surround of V1 neurons, and similar stimuli in human psychophysics, we find that near-surround suppression is more sharply orientation-tuned than far-surround suppression in both macaque V1 and human perception. These results point to a similarity between surround suppression in macaque V1 and human vision, and suggest that feedback circuits are less orientation-biased than horizontal circuits. We find sharpest tuning of near-surround suppression in V1 layers (3, 4B, 4Cα) with patterned and orientation-specific horizontal connections. Sharpest tuning of far-surround suppression occurs in layer 4B, suggesting greater orientation-specificity of feedback to this layer. Different orientation-tuning of near and far surround suppression may reflect a statistical bias in natural images, whereby nearby edges have higher probability than distant edges of being co-oriented and belonging to the same contour. Surround suppression would, thus, increase the coding efficiency of frequently co-occurring contours and the saliency of less frequent ones. Such saliency increase can help detect small orientation differences in nearby edges (for contour completion), but large orientation differences in distant edges (for directing saccades/attention).

Foveal and parafoveal contrast suppression are different: Mechanisms revealed by the study of healthy aging

“…Stimuli were presented parafoveally (68 eccentricity) with a near and far surround to enable comparison to single-cell neurophysiological studies in primate V1 (Shushruth et al, 2013) and infer possible neural underpinnings of age-related changes to surround suppression given that the near and far surround are suggested to arise from different anatomical circuitry (reviewed by Angelucci & Bressloff, 2006;Nurminen & Angelucci, 2014). Far surround suppression at V1 is fast in onset (Bair, Cavanaugh, & Movshon, 2003), has a large spatial extent (Levitt & Lund, 2002;Shushruth, Ichida, Levitt, & Angelucci, 2009), and is thought to arise exclusively from feedback connections from extrastriate cortex (Angelucci & Bressloff, 2006).…”

“…Far surround suppression at V1 is fast in onset (Bair, Cavanaugh, & Movshon, 2003), has a large spatial extent (Levitt & Lund, 2002;Shushruth, Ichida, Levitt, & Angelucci, 2009), and is thought to arise exclusively from feedback connections from extrastriate cortex (Angelucci & Bressloff, 2006). On the other hand, the near surround has narrower orientation tuning than the far surround (Shushruth et al, 2013) and receives multiple inputs: excitatory feedforward connections from LGN, intra-V1 inhibitory horizontal connections, and excitatory feedback connections from extrastriate cortex (Angelucci & Bressloff, 2006;Sceniak et al, 2006). Our finding that near but not far surround suppression was altered in the older participants suggests that extrastriate feedback contributions to the far surround are likely unaffected by normal aging.…”

“…Nearby edges are more likely than distant edges to be parallel and belong to the same physical contour (Field, Hayes, & Hess, 1993;Geisler, Perry, Super, & Gallogly, 2001). Orientation-specificity of near surround suppression (Shushruth et al, 2013) is therefore thought to remove homogenous visual information and allow detection of small orientation differences, which is useful for local contour integration in parafoveal vision (Petrov et al, 2005). Consequently, the fact that older adults demonstrate reduced near surround suppression of perceived contrast parafoveally predicts that older adults may have difficulties with tasks requiring contour integration.…”

“…Stimuli were matched to the perceptual contrast matching experiment of Shushruth et al (2013) ( Figure 1A). The target stimulus was a circular, horizontal sinusoidal grating (1 c/8) subtending 28 diameter and centered in the middle of the display.…”

Pattern Adaptation and Normalization Reweighting

“…Specifically, we used the steerable pyramid (Simoncelli et al, 1992;Portilla and Simoncelli, 2000), a subband image transform, to decompose each texture image into separate orientation and spatial-frequency channels. Each channel simulates the responses of a large number of linear receptive fields with the same spatial-frequency and orientation tuning.…”