Characteristics of surround inhibition in cat area 17

Abstract

The effects of stimuli falling outside the 'classical receptive field' and their influence on the orientation selectivity of cells in the cat primary visual cortex are still matters of debate. Here we examine the variety of effects of such peripheral stimuli on responses to stimuli limited to the receptive field. We first determined the extent of the classical receptive field by increasing the diameter of a circular patch of drifting grating until the response saturated or reached a maximum, and by decreasing the diameter of a circular mask in the middle of an extended grating, centred on the receptive field, until the cell just began to respond. These two estimates always agreed closely. We then presented an optimum grating of medium-to-high contrast filling the classical receptive field while stimulating the surround with a drifting grating that had the same parameters as the central stimulus but was varied in orientation. For all but five neurons (of 37 tested), surround stimulation produced clear suppression over some range of orientations, while none showed explicit facilitation under these conditions. For 11 cells (34% of those showing suppression), the magnitude of suppression did not vary consistently with the orientation of the surround stimulus. In the majority of cells, suppression was weakest for a surround grating oriented orthogonal to the cell's optimum. Nine of these cells (28%) exhibited maximum inhibition at the optimum orientation for the receptive field itself, but for 12 cells (38%) there was apparent 'release' from inhibition for surround gratings at or near the cell's optimum orientation and direction, leaving inhibition either maximal at angles flanking the optimum (9 cells) or broadly distributed over the rest of the orientation range (3 cells). This implies the existence of a subliminal facilitatory mechanism, tightly tuned at or near the cell's optimum orientation, extending outside the classical receptive field. For just two cells of 13 tested the preferred orientation for a central grating was clearly shifted towards the orientation of a surrounding grating tilted away from the cell's optimum. The contrast gain for central stimulation at the optimal orientation was measured with and without a surround pattern. For nine of 25 cells tested, surround stimulation at the cell's optimum orientation facilitated the response to a central grating of low contrast (< or =0.1) but inhibited that to a higher-contrast central stimulus: the contrast-response gain is reduced but the threshold contrast is actually decreased by surround stimulation. Hence the receptive field is effectively larger for low-contrast than for high-contrast stimuli. Inhibition from the periphery is usually greatest at or around the cell's optimum, while suppression within the receptive field has been shown to be largely non-selective for orientation. Inhibition by orientations flanking the optimum could serve to sharpen orientation selectivity in the presence of contextual stimuli and to enhance orientational contrast; and ...

Level Dependence of Contextual Modulation in Auditory Cortex

“…For low-contrast central stimuli, surround stimuli cause facilitation, whereas for high-contrast central stimuli, surround stimuli cause suppression (Polat et al 1998;Sengpiel et al 1997;Toth et al 1996). The facilitation is thought to depend on depolarizing synaptic inputs that can be evoked by stimuli outside the classical receptive field, as demonstrated by whole cell recordings (Bringuier et al 1999) and by imaging (Toth et al 1996).…”

“…In primary visual cortex and primary somatosensory cortex, context-dependent enhancement and suppression appear to depend on the relative level (or contrast) of the probe (Levitt and Lund 1997;Moore et al 1999;Polat et al 1998;Sengpiel et al 1997;Toth et al 1996). For high-level or high-contrast probes, contextual stimuli tend to cause suppression.…”

Surround Suppression of V1 Neurons Mediates Orientation-Based Representation of High-Order Visual Features

“…However, note that the former case is rarely found, since carrier orientation tunings for the CRF and surround are usually similar (Akasaki et al 2002;Blakemore and Tobin 1972;Nelson and Frost 1978;Walker et al 1999). Even if a neuron is more effectively suppressed by nonoptimal CRF orientations, it is likely that this neuron is suppressed by the CRF preferred orientation to some degree (Sengpiel et al 1997).…”

Intracortical Origins of Interocular Suppression in the Visual Cortex

“…Although the initial studies suggested that the responses of primary visual cortex (V1) neurons to an optimal stimulus are suppressed selectively by masking stimuli of orthogonal orientation, a consensus has emerged that a wide range of orientations can cause suppression, both within and outside the classical receptive field, with surround suppression in fact being strongest at the optimal orientation of the cell (Bonds, 1989;Nelson, 1991;DeAngelis et al, 1992;Li and Li, 1994;Sengpiel et al, 1997).…”