Dynamics of Suppression in Macaque Primary Visual Cortex

Abstract

The response of a neuron in primary visual cortex (V1) to an optimal stimulus in its classical receptive field (CRF) can be reduced by the presence of an orthogonal mask, a phenomenon known as cross-orientation suppression. The presence of a parallel stimulus outside the CRF can have a similar effect, in this case known as surround suppression. We used a novel stimulus to probe the time course of cross-orientation suppression and found that it is very fast, starting even before the response to optimal excitatory stimuli. However, it occurs with some delay after the offset response, considered to be a measure of the earliest excitatory signals that reach the CRF. We also examined the time course of response to a stimulus presented outside the CRF and found that cross-orientation suppression begins substantially earlier than surround suppression measured in the same cells. Together, these findings suggest that cross-orientation suppression is attributable to either direct feedforward signal paths to V1 neurons or a circuit involving fast local interneurons within V1. Feedback from higher cortical areas is implicated in surround suppression, but our results make this an implausible mechanism for cross-orientation suppression. We conclude that suppression from inside and outside the CRF occur through different mechanisms.

Sharper orientation tuning of the extraclassical suppressive-surround due to a neuron’s location in the V1 orientation map emerges late in time

“…To determine the evolution of the extraclassical surround over time, orientation tuning profiles of the surround were plotted at successive time points and SSI, ISD, Iso supp and Ortho supp were calculated for each. Responseonset was defined as the earliest time that the response to the stimulus reached 5% of its maximum with respect to spontaneous activity, similar to previous reports (Smith et al, 2006;Alitto and Usrey, 2008). Importantly, the response onset times of the optimal center alone, iso-surround, and orthosurround conditions did not vary significantly (p = 0.18, analysis of variance (ANOVA); see Fig.…”

Psychophysical evidence for two routes to suppression before binocular summation of signals in human vision

“…Although there are close comparisons between our psychophysical experiments on humans and single-cell work in cat (see above), little related work has been done in monkey (though see Smith et al, 2006) and analogous experiments have not been performed. Other work performed by Macknik and his colleagues (Tse et al, 2005;Macknik and Martinez-Conde, 2004) used a very different type of stimulus in which the mask and test contained similar oriented contours, but were not superimposed in either space or time.…”

“…Thus, if a subgroup of cells in V1 (e.g. in layer 4), were to share the crucial properties of cells in the LGN, we could not rule out the possibility that the broadband ipsiocular effects reside there (see also Smith et al, 2006;Webb et al, 2005).…”

“…For example, mask stimuli that drift or flicker too quickly to excite most cortical cells will nevertheless produce XOS, implying precortical involvement (Freeman et al, 2002;Sengpiel and Vorobyov, 2005). Possible origins include suppressive interactions in the lateral geniculate nucleus (LGN) (Levick et al, 1972;Bonin et al, 2005), saturation in the retina or LGN (Li et al, 2006;Priebe and Ferster, 2006;Smith et al, 2006) and depression at the thalamo-cortical synapse (Freeman et al, 2002). The last two accounts are applicable only when the mask and test are presented to the same eye (monoptic presentation) and overlap in space and time.…”

Feature attention evokes task-specific pattern selectivity in V4 neurons

“…This feature selectivity is usually manifest from the first spike of the response (2) and is assumed to be due to hard wiring in the network and to a certain extent a feed-forward process (3). When an animal searches for a visual target among distractors it is not unreasonable to assume that neurons in the brain will be selective for the search target, and we have recently shown that neurons in the lateral intraparietal area of the monkey (LIP) become selective for the target in a visual search task even when the monkey makes a saccade away from the receptive field (4).…”