Neuronal correlates of attentional selectivity and intensity in visual area V4 are invariant of motivational context

Flexibly switching attentional strategies is crucial for adaptive behavior in changing environments. Depending on the context, task demand employs different degrees of the two fundamental components of attention- attentional selectivity (preferentially attending to one location in visual space) and effort (the total non-selective intensity of attention). Neuronal responses in the visual cortex that show modulation with changes in either selective attention or effort are reported to partially represent motivational aspect of the task context. The relative contributions and interactions of these two components of attention to modulate neuronal signals and their sensitivity to distinct motivational drives are poorly understood. To address this question, we independently controlled monkeys' spatially selective attention and non-selective attentional intensity in the same experimental session during a novel visual orientation change detection task. Attention was controlled either by adjusting the relative difficulty of the orientation changes at the two locations or by the reward associated with stimuli at two locations while simultaneously recording spikes from populations of neurons in area V4. We found that V4 neurons are robustly modulated by either selective attention or attentional intensity. Notably, as attentional selectivity for a neuron's receptive field location decreased, its responses became weaker, despite an increase in the animal's overall attentional intensity. This strong interaction between attentional selectivity and intensity could be identified in single trial spike trains. A simple divisive normalization of spatially distributed attention performances can explain the interaction between attention components well at the single neuron level. The effects of attentional selectivity and attentional intensity on neuronal responses were the same regardless of whether the changes were motivated by reward or task difficulty. These results provide a detailed cellular-level mechanism of how fundamental components of attention integrate and affect sensory processing in varying motivational and stimulus contexts.

Clustered functional domains for curves and corners in cortical area V4

The ventral visual pathway is crucially involved in integrating low-level visual features into complex representations for objects and scenes. At an intermediate stage of the ventral visual pathway, V4 plays a crucial role in supporting this transformation. Many V4 neurons are selective for shape segments like curves and corners, however it remains unclear whether these neurons are organized into clustered functional domains, a structural motif common across other visual cortices. Using two-photon calcium imaging in awake macaques, we confirmed and localized cortical domains selective for curves or corners in V4. Single-cell resolution imaging confirmed that curve or corner selective neurons were spatially clustered into such domains. When tested with hexagonal-segment stimuli, we find that stimulus smoothness is the cardinal difference between curve and corner selectivity in V4. Combining cortical population responses with single neuron analysis, our results reveal that curves and corners are encoded by neurons clustered into functional domains in V4. This functionally-specific population architecture bridges the gap between the early and late cortices of the ventral pathway and may serve to facilitate complex object recognition.

Specialized contributions of mid-tier stages of dorsal and ventral pathways to stereoscopic processing in macaque

The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

Timing of response onset and offset in macaque V4: stimulus and task dependence

In the primate visual cortex, both the magnitude of the neuronal response and its timing can carry important information about the visual world, but studies typically focus only on response magnitude. Here, we examine the onset and offset latency of the responses of neurons in area V4 of awake, behaving macaques across several experiments, in the context of a variety of stimuli and task paradigms. Our results highlight distinct contributions of stimuli and tasks to V4 response latency. We found that response onset latencies are shorter than typically cited (median = 75.5 ms), supporting a role for V4 neurons in rapid object and scene recognition functions. Moreover, onset latencies are longer for smaller stimuli and stimulus outlines, consistent with the hypothesis that longer latencies are associated with higher spatial frequency content. Strikingly, we found that onset latencies showed no significant dependence on stimulus occlusion, unlike in inferotemporal cortex, nor on task demands. Across the V4 population, onset latencies had a broad distribution, reflecting the diversity of feedforward, recurrent and feedback connections that inform the responses of individual neurons. Response offset latencies, on the other hand, displayed the opposite tendency in their relationship to stimulus and task attributes: they are less influenced by stimulus appearance, but are shorter in guided saccade tasks compared to fixation tasks. The observation that response latency is influenced by stimulus- and task-associated factors emphasizes a need to examine response timing alongside firing rate in determining the functional role of area V4.

Specialization of mid-tier stages of dorsal and ventral pathways in stereoscopic processing

The division of labor between the dorsal and ventral visual pathways is an influential model of parallel information processing in the cerebral cortex. However, direct comparison of the two pathways at the single-neuron resolution has been scarce. Here we compare how MT and V4, mid-tier areas of the two pathways in the monkey, process binocular disparity, a powerful cue for depth perception and visually guided actions. We report a novel tradeoff where MT neurons transmit disparity signals quickly and robustly, whereas V4 neurons markedly transform the nature of the signals with extra time to solve the stereo correspondence problem. Therefore, signaling speed and robustness are traded for computational complexity. The key factor in this tradeoff was the shape of disparity tuning: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, this correlation between tuning shape and signal transformation was present across individual neurons within both MT and V4. Overall, our results reveal both distinct signaling advantages and common tuning-curve features of the dorsal and ventral pathways in stereoscopic processing.

Clustered Functional Domains for Curves and Corners in Cortical Area V4

The ventral visual pathway is crucially involved in integrating low-level visual features into complex representations for objects and scenes. At an intermediate stage of the ventral visual pathway, V4 plays a crucial role in supporting this transformation. Many V4 neurons are selective for shape segments like curves and corners, however it remains unclear whether these neurons are organized into clustered functional domains, a structural motif common across other visual cortices. Using two-photon calcium imaging in awake macaques, we confirmed and localized cortical domains selective for curves or corners in V4. Single-cell resolution imaging confirmed that curve or corner selective neurons were spatially clustered into such domains. When tested with hexagonal-segment stimuli, we find that stimulus smoothness is the cardinal difference between curve and corner selectivity in V4. Combining cortical population responses with single neuron analysis, our results reveal that curves and corners are encoded by neurons clustered into functional domains in V4. This functionally-specific population architecture bridges the gap between the early and late cortices of the ventral pathway and may serve to facilitate complex object recognition.

Patterns of neural correlations in visual cortex vary with the number of objects

How the brain preserves information about more than one stimulus at a time remains poorly understood. We recently showed that when more than one stimulus is present, single neurons may fluctuate between coding one vs. the other(s) across some time period. A critical unanswered question is whether and how any such fluctuations are coordinated across the neural population. Here, we analyzed the spike count (“noise”) correlations observed between pairs of visual cortex (V1, V4) neurons under a variety of conditions. We report that when two separate grating stimuli are presented simultaneously, distinct distributions of positive and negative correlations emerge in V1, depending on whether the two neurons in the pair both respond more strongly to the same vs. different individual stimuli. Neural pairs that shared the same stimulus preference were more likely to show positively correlated spike count variability whereas those with different preferences were more likely to show negative correlations, suggesting that the V1 population response to one particular stimulus may be enhanced over the other on any given trial. Distinct distributions of spike count correlations based on tuning preferences were also seen in V4 for adjacent stimuli, but were not observed in either structure for single stimuli or when the two gratings were superimposed and formed a single plaid. The effects were most pronounced among pairs of neurons that showed fluctuating activity. These findings support the interpretation that the pattern of correlated fluctuations is related to the segregation of individual objects in the visual scene.Significance StatementHow the brain separates information about multiple objects despite overlap in the neurons responsive to each item is not well understood. Here we show that pairs of neurons in primate V1 and V4 show unique patterns of correlated firing when there are multiple objects in the visual scene. These patterns were most pronounced in neurons that showed fluctuating activity consistent with switching between encoding each object across time (i.e. time division multiplexing). Both strongly positive and strongly negative correlations were observed, depending on whether the neurons in the pair exhibited similar or different stimulus preferences. These patterns were absent when only one object was presented, suggesting that they may play a key role in preserving information about multiple items.