Neurons in primary visual cortex, V1, very often have extra-classical receptive fields (eCRFs). The eCRF is defined as the region of visual space where stimuli cannot elicit a spiking response but can modulate the response of a stimulus in the classical receptive field (CRF). We investigated the dependence of the eCRF on stimulus contrast and orientation in macaque V1 cells for which the laminar location was determined. The eCRF was more sensitive to contrast than the CRF across the whole population of V1 cells with the greatest contrast differential in layer 2/3. We confirmed that many V1 cells experience stronger suppression for collinear than orthogonal stimuli in the eCRF. Laminar analysis revealed that the predominant bias for collinear suppression was found in layers 2/3 and 4b. The laminar pattern of contrast and orientation dependence suggests that eCRF suppression may derive from different neural circuits in different layers, and may be comprised of two distinct components: orientation-tuned and untuned suppression. On average tuned suppression was delayed by about 25 milliseconds compared to the onset of untuned suppression. Therefore, response modulation by the eCRF develops dynamically and rapidly in time.

Crowding is a profound loss of discriminability of visual features, when a target stimulus is surrounded by distractors. Numerous studies of human perception have characterized how crowding depends on the properties of a visual display. Yet, there is limited understanding of how and where stimulus information is lost in the visual system under crowding. Here, we show that macaque monkeys exhibit perceptual crowding for target orientation that is similar to humans. We then record from neuronal populations in monkey primary visual cortex (V1). These populations show an appreciable loss of information about target orientation in the presence of distractors, due both to divisive and additive modulation of responses to targets by distractors. Our results show that spatial contextual effects in V1 limit the discriminability of visual features and can contribute substantively to crowding.

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A key property of neurons in primary visual cortex (V1) is the distinction between simple and complex cells. Recent reports in cat visual cortex indicate the categorization of simple and complex can change depending on stimulus conditions. We investigated the stability of the simple/complex classification with changes in drive produced by either contrast or modulation by the extraclassical receptive field (eCRF). These two conditions were reported to increase the proportion of simple cells in cat cortex. The ratio of the modulation depth of the response (F1) to the elevation of response (F0) to a drifting grating (F1/F0 ratio) was used as the measure of simple/complex. The majority of V1 complex cells remained classified as complex with decreasing contrast. Near contrast threshold, an equal proportion of simple and complex cells changed their classification. The F1/F0 ratio was stable between optimal and large stimulus areas even for those neurons that showed strong eCRF suppression. There was no discernible overall effect of surrounding spatial context on the F1/F0 ratio. Simple/complex cell classification is relatively stable across a range of stimulus drives, produced by either contrast or eCRF suppression.

Complex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. Although much is known about V1 eCRF properties, we do not yet know how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.