Functional Clusters of Neurons in Layer 6 of Macaque V1.

Layer 6 appears to perform a very important role in the function of macaque primary visual cortex, V1, but not enough is understood about the functional characteristics of neurons in the layer 6 population. It is unclear to what extent the population is homogeneous with respect to their visual properties or if one can identify distinct subpopulations. Here we performed a cluster analysis based on measurements of the responses of single neurons in layer 6 of primary visual cortex in male macaque monkeys (Macaca fascicularis) to achromatic grating stimuli that varied in orientation, direction of motion, spatial and temporal frequency, and contrast. The visual stimuli were presented in a stimulus window that was also varied in size. Using the responses to parametric variation in these stimulus variables, we extracted a number of tuning response measures and used them in the cluster analysis. Six main clusters emerged along with some smaller clusters. Additionally, we asked whether parameter distributions from each of the clusters were statistically different. There were clear separations of parameters between some of the clusters, particularly for f1/f0 ratio, direction selectivity, and temporal frequency bandwidth, but other dimensions also showed differences between clusters. Our data suggest that in layer 6 there are multiple parallel circuits that provide information about different aspects of the visual stimulus.SIGNIFICANCE STATEMENT The cortex is multilayered and is involved in many high-level computations. In the current study, we have asked whether there are subpopulations of neurons, clusters, in layer 6 of cortex with different functional tuning properties that provide information about different aspects of the visual image. We identified six major functional clusters within layer 6. These findings show that there is much more complexity to the circuits in cortex than previously demonstrated and open up a new avenue for experimental investigation within layers of other cortical areas and for the elaboration of models of circuit function that incorporate many parallel pathways with different functional roles.

Functional characterization of the extraclassical receptive field in macaque V1: contrast, orientation, and temporal dynamics.

Neurons in primary visual cortex, V1, very often have extraclassical 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 ∼25 ms compared with the onset of untuned suppression. Therefore, response modulation by the eCRF develops dynamically and rapidly in time.

Stability of simple/complex classification with contrast and extraclassical receptive field modulation in macaque V1.

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.

Feature representation under crowding in macaque V1 and V4 neuronal populations.

Visual perception depends strongly on spatial context. A profound example is visual crowding, whereby the presence of nearby stimuli impairs the discriminability of object features. Despite extensive work on perceptual crowding and the spatial integrative properties of visual cortical neurons, the link between these two aspects of visual processing remains unclear. To understand better the neural basis of crowding, we recorded activity simultaneously from neuronal populations in V1 and V4 of fixating macaque monkeys. We assessed the information available from the measured responses about the orientation of a visual target both for targets presented in isolation and amid distractors. Both single neuron and population responses had less information about target orientation when distractors were present. Information loss was moderate in V1 and more substantial in V4. Information loss could be traced to systematic divisive and additive changes in neuronal tuning. Additive and multiplicative changes in tuning were more severe in V4; in addition, tuning exhibited other, non-affine transformations that were greater in V4, further restricting the ability of a fixed sensory readout strategy to extract accurate feature information across displays. Our results provide a direct test of crowding effects at different stages of the visual hierarchy. They reveal how crowded visual environments alter the spiking activity of cortical populations by which sensory stimuli are encoded and connect these changes to established mechanisms of neuronal spatial integration.

Spatial contextual effects in primary visual cortex limit feature representation under crowding.

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.

Distinct spatiotemporal mechanisms underlie extra-classical receptive field modulation in macaque V1 microcircuits.

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.

Inconsistent channel bandwidth estimates suggest winner-take-all nonlinearity in second-order vision.

The processing of texture patterns has been characterized by a model that postulates a first-stage linear filter to highlight a component texture, a pointwise rectification stage to convert contrast for the highlighted texture into mean response strength, followed by a second-stage linear filter to detect the texture-defined pattern. We estimated the spatial-frequency bandwidth of the second-stage filter mediating orientation discrimination of orientation-modulated second-order gratings by measuring threshold elevation in the presence of filtered noise added to the modulation signal. This experiment yielded no evidence for frequency tuning. A second experiment, in which subjects had to detect similar second-order gratings while judging their modulation frequency, produced bandwidth estimates of 1-1.5 octaves, similar to estimated bandwidths of first-order channels. We propose that an additional dominant-response-selection nonlinearity can account for these apparently contradictory results.