In macaque primary visual cortex (V1) neuronal responses to stimuli inside the receptive field (RF) are modulated by stimuli in the RF surround. This modulation is orientation-specific. Previous studies suggested that for some cells this specificity may not be fixed, but changes with the stimulus orientation presented to the RF. We demonstrate, in recording studies, that this tuning behavior is instead highly prevalent in V1 and, in theoretical work, that it arises only if V1 operates in a regime of strong local recurrence. Strongest surround suppression occurs when the stimuli in the RF and the surround are iso-oriented, and strongest facilitation when the stimuli are cross-oriented. This is the case even when the RF is sub-optimally activated by a stimulus of non-preferred orientation, but only if this stimulus can activate the cell when presented alone. This tuning behavior emerges from the interaction of lateral inhibition (via the surround pathways), which is tuned to the RF’s preferred orientation, with weakly-tuned, but strong, local recurrent connections, causing maximal withdrawal of recurrent excitation at the feedforward input orientation. Thus, horizontal and feedback modulation of strong recurrent circuits allows the tuning of contextual effects to change with changing feedforward inputs.

Neuronal responses in primary visual cortex (V1) to optimally oriented high-contrast stimuli in the receptive field (RF) center are suppressed by stimuli in the RF surround, but can be facilitated when the RF center is stimulated at low contrast. The neural circuits and mechanisms for surround modulation are still unknown. We previously proposed that topdown feedback connections mediate suppression from the "far" surround, while "near" surround suppression is mediated primarily by horizontal connections. We implemented this idea in a recurrent network model of V1. A model assumption needed to account for the contrast-dependent sign of surround modulation is a response asymmetry between excitation and inhibition; accordingly, inhibition, but not excitation, is silent for weak visual inputs to the RF center, and surround stimulation can evoke facilitation. A prediction stemming from this same assumption is that surround suppression is weaker for low than for high contrast stimuli in the RF center. Previous studies are inconsistent with this prediction. Using single unit recordings in macaque V1, we confirm this model's prediction. Model simulations demonstrate that our results can be reconciled with those from previous studies. We also performed a systematic comparison of the experimentally-measured surround suppression strength with predictions of the model operated in different parameter regimes. We find that the original model, with strong horizontal and no feedback excitation of local inhibitory neurons, can only partially account quantitatively for the experimentally-measured suppression. Strong direct feedback excitation of V1 inhibitory neurons is necessary to account for the experimentally-measured surround suppression strength.